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Aus dem Institut für Tierzucht und Tierhaltung der Agrar- und Ernährungwissenschaftlichen Fakultät der Christian-Albrechts-Universität zu Kiel NUTRIENT FLUXES IN MULTITROPHIC AQUACULTURE SYSTEMS Dissertation zur Erlangung des Doktorgrades der Agrar- und Ernährungwissenschaftlichen Fakultät der Christian-Albrechts-Universität zu Kiel vorgelegt von Master of Science YUDI NURUL IHSAN aus Bandung - Indonesien Kiel, 2012 Dekanin: Prof. Dr. K. Schwarz Erster Berichterstatter: Prof. Dr. C. Schulz Zweiter Berichterstatter: Prof. Dr. E. Hartung Tag der mündlichen Prüfung: 09.02.2012

NUTRIENT FLUXES IN MULTITROPHIC AQUACULTURE SYSTEMS · The contribution of fish to global human food supply has reached a record of about 17 kg per person in average, supplying over

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Page 1: NUTRIENT FLUXES IN MULTITROPHIC AQUACULTURE SYSTEMS · The contribution of fish to global human food supply has reached a record of about 17 kg per person in average, supplying over

Aus dem Institut für Tierzucht und Tierhaltung

der Agrar- und Ernährungwissenschaftlichen Fakultät

der Christian-Albrechts-Universität zu Kiel

NUTRIENT FLUXES IN MULTITROPHIC

AQUACULTURE SYSTEMS

Dissertation

zur Erlangung des Doktorgrades

der Agrar- und Ernährungwissenschaftlichen Fakultät

der Christian-Albrechts-Universität zu Kiel

vorgelegt von

Master of Science

YUDI NURUL IHSAN

aus Bandung - Indonesien

Kiel, 2012

Dekanin: Prof. Dr. K. Schwarz

Erster Berichterstatter: Prof. Dr. C. Schulz

Zweiter Berichterstatter: Prof. Dr. E. Hartung

Tag der mündlichen Prüfung: 09.02.2012

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Gedruckt mit Genehmigung der Agrar- und Ernährungswissenschaftlichen

Fakultät der Christian-Albrechts-Universität zu Kiel

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  III

Table of Contents

General Introduction ....................................................................................................... 1

Chapter 1:

Nutrient flux in polyculture system using seaweed as biofilter: Implication for

sustainability............................................................................................................... 5

Chapter 2:

A Comparison of nutrient fluxes in monoculture and polyculture systems for

shrimp (Penaeus vannamei) and seaweed (Gracillaria verrucosa) production...... . 20

Chapter 3:

Nutrient Fluxes and Mass Balances in Various Polyculture Systems Using

Shrimp Penaeus vannamei, Fish Oreochromis sp. and Seaweed Gracillaria

verrucosa ................................................................................................................. 46

Chapter 4:

Nitrogen Assimilation Potential of Seaweed Gracillaria verrucosa in

Polyculture with Pacific White Shrimps (Penaeus vannamei) .............................. 74

General Discussion ...................................................................................................... 95

General Summary......................................................................................................... 102

Zusammenfassung........................................................................................................ 104

Danksagung.................................................................................................................. 107

Lebenslauf .................................................................................................................... 108

 

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General Introduction

The marine sector including aquaculture is one of the leading sectors in economic

development in the world. Aquaculture contributes significantly to food

availability, household food security, income generation, trade, and improved

living standards in Indonesia. In poor rural communities, aquaculture can be an

integral component of development contributing to sustainable livelihoods and

enhancing social well-being. Since 1990 the gap between the demand for and

supply of fish has been widening rapidly due to the decline of capture fisheries

production and a continually growing population. Aquaculture is forecasted to

dominate, if not surpass, the importance of marine capture fisheries in providing

high quality animal protein to lower income groups, employment, and export

earnings.

Indonesia has good fisheries and aquaculture potential. Because of its rich, coastal

and marine resources suitable for aquaculture development, it is one country

where aquaculture can contribute to economic and social development goals. The

potential area for aquaculture is estimated at about 26 million hectares (ha),

consisting of 24.5 million ha of coastal areas suitable for mariculture, 913

thousand ha of brackish water areas, and 1.1 million ha of freshwater areas.

Actual area coverage of aquaculture is currently estimated at only 681 thousand

ha, corresponding to less than 3% of the total potential area.

The contribution of fish to global human food supply has reached a record of

about 17 kg per person in average, supplying over three billion people with at

least 15% of their average animal protein intake (FAO, 2010). Marine aquaculture

has been a rapidly growing industry, increasing from about 18.6 million tons in

2006 to 20.1 million tons in 2009 and these patterns are expected to continue up to

2030 due to the increasing global demand and high market value of aquaculture

products (FAO, 2010). Global production of shrimp has increased by more than

600% between 1989 and 2009 and is expected to continue due to the high market

value of cultured shrimp. This production comes from a variety of farms ranging

from small-scale ponds to large-scale ponds.

As a result of the rapid production increase, it is not unreasonable to conceive that

aquaculture activities might affect the environment in a variety of ways, especially

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fish and shrimp aquaculture which need to supplemented with an exogenous

source of nutrients. Increased production is being achieved by expansion of land

and water areas under culture and involve higher utilization of production inputs

such as water, feeds, fertilizers, and chemicals. Higher inputs normally affect the

surrounding environment in a number of ways. Particular concern arise by the

effects of particulate nitrogeneous wastes produced by the ponds in the form of

uneaten feed and fish faeces (Pearson and Gowen, 1990; Troell et al., 2003).

Poorly managed coastal shrimp farms have been cited for degrading nearshore

habitats through nutrient enrichment (Boyd, 1999; Hargreaves, 1998). Nutrient

enrichment could also affect the shrimp farms themselves through self-pollution.

Poor water quality may reduce farm productivity by diminishing shrimp growth

and/or promoting shrimp disease outbreaks (Hargreaves, 1998; Lin, 1989).

Identifying aquaculture species and system that are expected to be profitable is an

essential step toward developing sustainable aquaculture and to decrease the

adverse impact (Andersen, 2002 in Leung et al., 2007). Asian countries have been

practicing polyculture systems, through trial and error and experimentation for

centuries (Qian et al., 1996). These strategies were motivated by the need to

maximize productivity per unit of land and water bodies. They were based on

diversified self-reliance in feed and basic raw material production and the

philosophy that the by-products (wastes) from one resource use must become an

input of another resource in use (Chopin et al., 2001; Neori et al., 2004). On the

other hand polyculture has disadvantage as it could decrease main target

organisms production due to competition in space and nutrient utilization with co-

cultured organisms.

Shrimp Penaeus vannamei, seaweed Gracillaria verrucosa and fish Oreochromis

sp. had been used in presented thesis due to the different trophic level they

inhabitated, the high economic value, and well developed knowledge of

cultivation. Hypothesis of this study are: (1) nutrient given to the ponds can be

used most efficiently by polyculture system, (2) polyculture system using shrimp,

seaweed and fish can be used to minimize adverse impact of aquaculture to the

environment, (3) seaweed Gracillaria verrucosa can be used to absorb nutrient

excretion from shrimp and fish wastes and may contribute to the oxygen budget.

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To prove this hypothesis, in Chapter 1 of present study, based on a literature

review polyculture system can be described as the practice of culturing more than

one aquatic organism in the same system. In Chapter 2, empiricial calculations of

nutrients fluxes and mass balances in monoculture and polyculture systems with

shrimp Penaeus vannamei and seaweed Gracillaria verrucosa were realized and

compared. Additional investigations were conducted in Chapter 3 to determine

nutrient fluxes and mass balances in various polyculture systems using shrimp

Penaeus vannamei, Fish Oreochromis sp. and Seaweed Gracillaria verrucosa.

Finally, in Chapter 4, nitrogen assimilation potential of seaweed Gracillaria

verrucosa in polyculture with pacific white shrimps Penaeus vannamei was

estimated.

References

Boyd, C. E. 1999. Codes of Practise for Responsible Shrimp Farming. Global

Aquaculture Alliance. St. Louis MO. USA. 48.

Chopin, T., A. H Buschmann, C. Halling, M Troell, N Kautsky, A. Neori, G.

Kraemer, J. Zertuche-Gonzalez, C. Yarish, C. Neefus. 2001. Integrating

seaweeds into aquaculture systems: a key towards sustainability. J Phycol

37:975–986.

FAO. 2010. The state of world fisheries and aquaculture. Fisheries and

aquaculture department. Food and Agriculture Organization of United

Nations. Rome. Italy.

Hargreaves, J.A. (1998). Nitrogen biogeochemistry of aquaculture ponds.

Aquaculture 166, 181–212.

Neori, A., T. Chopin T, M. Troell, A. H. Buschmann, G.P. Kraemer, C. Halling,

M. Shpigel, C Yarish. 2004. Integrated aquaculture: rationale, evolution

and state of the art emphasizing seaweed biofiltration in modern

mariculture. Aquaculture 231:361–391.

Pearson, T. H., and R. J. Gowen. 1990. Impact of caged fish farming on the

marine environment – the Scottisch experience, 9-13. In interactions

between aquaculture and the environment, vol. An Taisce - The National

Trust for Ireland, Dublin.

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Troell M, C. Halling, A. Neori, T. Chopin, A. H. Buschmann, N. Kautsky, C.

Yarish. 2003. Integrated mariculture: asking the right questions.

Aquaculture 226:69–90.

Qian, P. Y., C. Y. Wu, M. Wu, Y. K. Xie. 1996. Integrated cultivation of red alga

Kappaphycus alvarezii and the pearl oyster Pinctada martensi.

Aquaculture 147: 21-35

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

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Chapter 1: Nutrient Flux in Polyculture System Using Seaweed as

Biofilter: Implications for Sustainability (Mini Review)

Y. N. Ihsanab, K. J. Hessec, C. Schulzab

aGesellschaft für Marine Aquakultur mbH, Hafentörn 3, D-25761 Büsum

bInstitute for Animal Breeding and Husbandry, Christian-Albrechts-Universität

D-24098 Kiel

cResearch and Technology Centre, Christian-Albrechts-Universität

D-25761 Büsum

Submitted to the Journal of Asian Fisheries Society

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Abstract

In general, feed based shrimp and fish aquaculture can produce a large amount of

waste, including nitrogen and phosphorus that is released to the aquatic

environment without treatment. One of the main environmental issues is the direct

discharge of significant nutrient loads into coastal waters from aquaculture ponds

system. In its search for best management practices, the aquaculture industry

should develop innovative and responsible practices that optimize its efficiency

and create diversification, while ensuring the remediation of the consequences of

its activities to maintain the health of coastal waters. At present, seaweed

cultivation in integrated polyculture system appears to be a viable approach to

reduce discharge nutrients to the environment. By integrating fed aquaculture, the

wastes of one resource user become a resource for the others (Neori et al., 2004).

Seaweed can be efficient at removal of nutrients from effluent of intensive fish

farm (Troell et al., 1997; Neori et al., 2004). The production of seaweed in cage

culture can be successfully integrated with production of fish and shrimp.

Regarding the environmental benefits of integrated seaweed and fish or shrimp

production, seaweed culture can also benefit by increasing their economic

viability. Integrated seaweed aquaculture systems have been suggested as a

possible solution for securing an increasing and environmentally sounded

production of future supply of fish and seafood.

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Introduction

Aquaculture has expanded rapidly all over of the world, especially in tropical

areas which account for 89% of production in terms of quantity and 79% in terms

of value (FAO, 2010). Aquaculture production (excluding seaweed) was less than

1 million tons per year in the early 1950, production in 2008 already achieved

52.5 million tons, with a value of US$ 98.4 billion. Seaweed production by

aquaculture in 2008 was 15.8 million tons (live weight equivalent), with a value

of US$7.4 billion, representing an average annual growth rate in terms of weight

of almost 8% since 1970. If seaweed is included, total global aquaculture

production in 2008 amounted to 68.3 tons with a first-sale value of US$ 106

billion (FAO, 2010). It is expected that world aquaculture production will

continue to grow in the coming decade. Aquaculture is a source of income and

livelihood for millions of people around the world. Employment in fisheries and

aquaculture has grown substantially in the last three decades, with an average rate

of increase of 3.6% per year since 1980 (FAO, 2010).

The expansion of aquaculture has brought concern about the possible effect of

aquaculture effluents on coastal ecosystem. Aquaculture has contributed to

environment degradation, with visible effect such as increases in particulate

organic matter and chemical change such as dissolved oxygen reduction and

increased nitrogen and phosphorus concentrations in water (Troell et al., 1999).

The negative impact of aquaculture on the environment due to the release of

nitrogen and phosphorus is related to eutrophication processes, especially in

coastal and sheltered areas (Neori et al., 2000; Neori and Shpigel, 2003). This

nutrient release is primarily caused by intensive and semi intensive production of

fish. Feed and fertilizer which are applied in ponds are not fully incorporated into

the cultured species partly deposited in pond sediments or discharged as effluents.

In average, fish or shrimp assimilates only 23-31% of nitrogen and 10-13% of

phosphorus of the total inputs and remaining 14-53% of nitrogen and 39-67% of

phosphorus are deposited in the sediment (Neori et al., 2000; Dhirendra and Lin,

2002; Schuenhoff et al., 2003). Nutrient in aquaculture effluents are distributed in

a particulate or soluble fraction (Ackefors and Enell, 1994). In fresh manure,

about 7-32% of total nitrogen (TN) and 30-84% of total phosphorus (TP) are

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bound in this particulate fraction and the remainder are excreted in dissolved

forms (Bergheim et al., 1993). In intensive marine shrimp culture, only 24% and

13% of dietary nitrogen and phosphorus were incorporated into harvested shrimp,

while the remaining nutrients were released into the surrounding water (Briggs

and Funge-Smith, 1994). Phosphorus releases were estimated to be 9.4 kg

(Ackefors and Enell, 1990) and 19.6–22.4 kg (Holby and Hall, 1991) per ton of

shrimp produced. This release may cause environmental and socio-economic

problems (Troell et al., 1999). The future aquaculture must be based on the

development of sustainable environmentally sounded production techniques

(Neori et al., 2004).

In recent years, integrated aquaculture has been proposed as a mean to reduce the

nutrient loading from aquaculture, including the improvement of feed utilization

by animals. Feed aquaculture (e.g. finfish, shrimp) needs to be integrated with

organic and inorganic extractive aquaculture (e.g. shellfish and seaweed). Schulz

et al. (2003) reported the total suspended solids (TSS) were reduced by 95.8-

97.3% from rainbow trout farm effluent in constructed wetland with emergent

plants and subsurface horizontal water flow. This nutrient incorporation of co-

cultured organisms of different trophic levels is the basis of environmentally

sounded aquaculture (Chopin et al., 2001; Neori et al., 2004). Integrated

aquaculture provides nutrient bioremediation, mutual benefits to the co-cultured

organisms, economic diversification and increased profitability. Ideally, nutrient

process in polyculture system with two or more ecologically compatible species

should be balanced, waste from one species are recycled as fertilizer or feed by

another without conflicting with each other (Neori et al., 2000).

The aim of this paper is to present and discuss the nutrient fluxes from various

polyculture systems on coastal waters. Additionally, comparative studies in this

paper provide evidence that polyculture represents a promising technique relative

to conventional monoculture for the production of aquaculture.

Polyculture system

Polyculture is the practice of culturing more than one species of aquatic organism

in the same pond. The motivating principle is that fish production in ponds may

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be maximized by raising a combination of species having different food habits.

The concept of polyculture of fish is based on the concept of total utilization of

different trophic and spatial niches of a pond in order to obtain maximum fish

production per unit area (Edward, 1992; Chiang, 1993; Qian et al., 1996). The

mixture of fish gives better utilization of available natural food produced in a

pond. The compatible fish species having complimentary feeding habits are

stocked so that all the ecological niches of pond ecosystem are effectively

utilized. The possibility of increasing fish production per unit area, through

polyculture, is considerable, when compared with monoculture system of fish.

Different species combination in polyculture system effectively contributes also to

improve the pond environment (Buschmann, 1996; Schuenhoff et al., 2003; Matos

et al., 2006).

Ponds that have been enriched through chemical fertilization, manuring or feeding

practices contain abundant natural fish food organisms living at different depths

and locations in the water column. Most fish feed predominantly on selected

groups of these organisms. Polyculture should combine fish having different

feeding habits in proportions that effectively utilize these various natural feed

items (Figure 1). As a result, higher yields are obtained (Bocek, unpublished).

Figure 1: Polyculture utilizes natural foods efficiently

(source: Bocek, unpublished)

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Shrimp ponds are traditionally set up in marine coastal areas and can lead to

adverse impact on the environment, especially of large areas of mangrove forest.

Cage culture can be a more sustainable alternative for rearing shrimp and

polyculture with seaweed may also improve sustainability.

Table 1. Worldwide polyculture system

Species Location Objective References

Shrimp (Penaeus monodon)

and Milkfish (Chanos

chanos)

Thailand To compare shrimp

performance

between mono and

polyculture system

Kuntiyo and Balio,

1997

Abalone (Haliotis

tuberculata), fish, and

seaweed (Ulva lactuca)

Israel To evaluated N-

budgets and fish

performance

Neori et al., 1998

Tilapia and shrimp Thailand To increase fish

production

Yi et al., 2003

Fish (Sparus aurata and

seaweed (Ulva. lactuca)

Portugal To evaluated the

performance of

ponds with effluent

through seaweed

Schuenhoff et al.,

2003

Shrimp (Litopenaeus

vannamei) and seaweed

(Kappaphycus alvarezii)

Brazil To test the

feasibility of co-

culturing shrimp

and seaweed

Lombardi et al.,

2006

Table 1 show the worldwide various polyculture systems that have been done by

several researchers. Kuntiyo and Balio (1997) reported after 109 culture days,

results showed no significant difference (P>0.05) on growth and survival rates of

both commodities in two culture schemes. Mean weight gain was 30.88 g for

shrimp and 263.33 g for milkfish in monoculture and 31.85 g and 210.57 g for

shrimp and milkfish, respectively, in the polyculture system. Mean survival rates

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were 94.03% for shrimp and 99.0% for milkfish in monoculture; and 82.13% for

shrimp and 92.33% for milk-fish for the polyculture system. Net aggregate

production, however, was highly significant in polyculture, attaining 923.50

kg/ha/crop. Economic feasibility revealed encouraging results for polyculture over

monoculture, with return on investment (ROI) valued at 45% for polyculture.

Nutrient flux

The two significant components of the pond environment are the pond water and

sediment which interact continuously to influence the culture environment. Pond

sediment can be further divided into the pond soil component (the pond bottom

and walls) and the accumulated sediment component (Briggs and Funge-Smith,

1994).

Nutrient budget are derived for solid, particulate organic matter, nitrogen, and

phosphorus. The erosion of pond soil is the major source of solid budget and

organic matter in the pond. The feed applied to the pond is a significant source of

organic matter (31-50%) in the pond but contributed little amount of solids (4-7%)

to the system (Funge-Smith and Briggs, 1998). This is important since the feed

component is also an indication of the faecal contribution by fish or shrimp.

Funge-Smith and Stewart (1996) reported the nitrogen budgets reveal in more

detail, the source and sinks of the organic components in an intensive shrimp pond

(Table 2). Applied feed accounted for 78% of the input N to the ponds. Erosion of

the pond soils, whilst a major contributor of solid, accounted for only 16% of

added to the system. Other minor contribution was influent water (4.03%), and

fertilizer, rainfall, shrimp stocked (2%). The sinks for nitrogen were the sediments

(24%), harvested shrimp (18%), and discharged water (28%). This leaves

approximately 30% of the nitrogen unaccounted for which is assumed to be N lost

to the atmosphere as N2.

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Table 2. Nitrogen budget for intensive shrimp ponds (Funge-Smith and Stewart,

1996)

Source and sinks Nitrogen (%)

Nitrogen input

Feed 78

Fertilizer 1.8

Rainfall 0.12

Shrimp stocked 0.02

Influent water 4.03

Erosion of pond soil 16

Nitrogen output

Sediment removal 24

Shrimp harvest 18

Water outflow 17

Harvest drainage 11

Denitrification 30

Application of seaweed to polyculture system

The use of seaweed integrated with fish cultures has been studied in open water

and land-based system condition in Israel, Portugal, Brazil, and Indonesia (Neori

et al., 1998; Schuenhoff et al., 2003; Lombardi et al., 2006). General concepts

about nutrient uptake by seaweed can be found in Harrison and Hurd (2001). To

optimize the seaweed component of an integrated aquaculture system, particular

attention should be given not only to physical and chemical factors such as light,

temperature, effluent nutrient concentration and flux, and water motion but also

biological factors such as interplant variability, nutrient prehistory, type of plant

tissue and age.

A pilot scale system for the intensive abalone in polyculture system was

established aimed at eliminating the dependence on external feed source and

nutrient discharge levels. Effluents from abalone (Haliotis tuberculata) culture

tanks drained into seaweed (Ulva lactuca) culture and biofilter tanks. Nitrogenous

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waste products by abalone contributed to the nutrition of seaweed. The abalone

grew on average 0.26%/d and mean seaweed production amounted 230 g/m2/d.

Nitrogen supplied was removed on average 58% (Neori et al., 1998).

Polyculture system consisted of fish and seaweed was evaluated by Schuenhoff et

al. (2003). An intensive fishpond (Sparus aurata) and three stage seaweed Ulva

lactuca biofilter were used which recirculated 50% of the effluent back to the

fishpond. Seaweed mean production was 94 g/m2/day. Nitrogen content of Ulva

lactuca was 34% of dry weight. Seaweed Ulva lactuca can remove 30% of

dissolved nutrient load from fishpond.

There were no negative interferences in co-culturing shrimp and seaweed inside

the same cage. Lombardi et al. (2006) reported no significant difference (P>0.05)

between two treatment (monoculture and polyculture with seaweed) for shrimp

weight gain, food conversion rate (FCR), and survival rate. Shrimp yield reached

production rates of 3.23 kg/m2/a and seaweed Kappaphycus alvarezii production

reached rates as high as 23.70 kg/m2/a. It means seaweed is able to grow inside

shrimp cage (Table 3).

Seaweed can also be a useful tool for measuring the zone of influence of an

aquaculture site, because they are integrators of bioavailable nutrients over time

(Troell et al., 1997). Jimenez del Rio (1994) found that increasing ammonium

loading rates per unit area of Ulva lactuca tank cultures fed with fish effluents led

to decrease dissolved nitrogen efficiency but increased nitrogen area uptake rate.

Seaweed yield and protein content also increased with increasing ammonium

supply per unit area. The same conclusion as ammonium uptake efficiency

decreased with the water turnover rate but the uptake per gram of Gracillaria per

time increased (Troell et al., 1997). Seaweed performs better as nitrogen absorber

with ammonium than with nitrate which is excellent in context on intensive fish

aquaculture where most of nitrogen is released as ammonium (Carmona et al.,

2001).

Review of result

Polyculture systems using seaweeds for the removal or conversion of wastes has

been done together with shrimp or fish. Lombardi et al. (2006) calculated the

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mean relative growth rate (RGR) for seaweed is 0.80-1.30%/day. This value is

lower compared to the others (Table 3). The highest RGR is nearly 3.00%/day

reported by Eswaran et al. (2002). The result suggest that depth is the main factor

that affects the growth of seaweed, because in most of the experiment higher RGR

were observed on surface floating ropes, whereas the lowest RGR from Lombardi

et al. (2006) were cultured at different depth between 1 – 2 m.

Table 3. Relative growth rate (RGR) of seaweed in various studies (Lombardo et

al., 2006)

RGR (%) Condition Reference

0.80 – 1.30 Inside cages Lombardy et al., 2006

3.72 – 7.17 Inside cages Hurtado-Ponce, 1992

8.00 – 10.00 Outside cages Rincones and Rubio,

1998

4.00 – 8.00 Outside cages Ohno et al., 1999

2.30 – 4.20 Outside cages Hurtado et al., 2001

6.50 – 10.70 Outside cages De Paula et al., 2001

Nearly 3.00 Outside cages Eswaran et al., 2002

During the last decade, renewed interest in incorporating seaweed as a biofilter

link in integrated carnivore-herbivore polyculture system has produce new

approach and practical technologies (Troell et al., 1999; De Paula et al., 2002;

Eswaran et al., 2002; Lombardi et al., 2006). These studies indicate that seaweeds

especially Gracillaria sp. can assimilate as much as 5-20% of the ammonium

produced by intensive fish or shrimp culture (Lombardi et al., 2006).

The main issue in the effective implementation of polyculture systems is their

optimal functioning, which requires an in-depth understanding of the physiology

and nutrition of the selected species. With seaweed, like with many organisms, the

different physiological processes taking place have different environmental

requirements (Harrison and Hurd, 2001). Consequently, the optimization of the

overall efficiency of a cultivation system can be complex because it will require a

compromise between apparently conflicting objective e.g. biomass or particular

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compound production versus bioremediation efficiency (Chopin and Yarish,

1998). For example, growth, nutrient uptake, carrageenan (agar production), and

phycocolloid quality respond differentially to nutrient enrichment (Buschmann et

al., 2001).

In tank culture, nutrient availability can be controlled by changing the water flow.

By increasing the water flow, nutrient flux will increase as well, which allows a

high biomass production of nutrient-sufficient seaweeds. In the other side, the

nutrient uptake efficiency is low and nutrient concentration remains high in the

effluents. If the water flow is low, nutrients become limiting and seaweed biomass

production decreases, but the nutrient uptake efficiency is higher (Hanisak, 1998).

If seaweed is only used as a biofilter and identified low commercial value species

like Ulva lactuca, they can be used to depurate fish effluents (Schuenhoff et al.,

2003). However, this apparent bioremediation merely shifts the problem of waste

disposal as the seaweed scrubber will in turn need to be disposed of or treated. On

the other hand, species like Gracilaria sp., Porphyra sp., or Laminaria sp. offer

both high bioremediation efficiency and commercial value in established market

such as human consumption (Neori and Shpigel, 1999).

When the value added for the service of improving water quality and coastal

health is finally recognized, quantified and combined with that of the principal

crop (shrimp aquaculture), the seaweed component of a polyculture system will be

understood to significantly improve the success of a diversified operation. An

accrued benefit to operators of polyculture system is the fact that the currently

discharge (unassimilated or excreted) nitrogen and phosphorus, which represent a

loss of money in real terms, will be captured and converted into the production of

salable biomass and bioproducts, hence generating revenues that may more than

compensate for the expenses. Additionally, as legislative guidelines, standards,

and controls regarding the discharge of inorganic nutrients into coastal waters

become more stringent in many countries and for sustainable aquaculture,

bioremediation via the production of seaweeds will help the shrimp aquaculture

industry and avoid noncompliance.

To successfully develop integrated aquaculture system, much research and

development remains to be undertaken, particularly in the following areas:

  15

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1. Transfer and modification of cultivation technologies to local environments

and socioeconomics,

2. development of the cultivation of native species of marketable value that will

be fast growing at different times of the year and in diverse habitats,

3. site-specific biological, chemical, physical, and socioeconomic modelling to

define the appropriate proportions between the different co-cultured

organisms.

Conclusions

Responsible aquaculture practices should be based on balanced ecosystem

management approach, the basic premise of which is to incorporate the biological

and environmental function of a diverse group of organisms into a unified system

that maintains the natural interaction of species and allows an ecosystem to

function sustainably. To help and to ensure its sustainability, however, it needs to

responsibly change its too often monoculture practices by adopting polyculture

ones to become better integrated into broader coastal management framework.

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Schulz, C., J. Gelbrecht, B. Rennert. 2003. Treatment of rainbow trout farm

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horizontal water flow. Aquaculture. Elsevier. 217: 207-221.

Troell, M., C Halling, A Nilsson, A. H Buschmann., N Kautsky, L Kautsky. 1997.

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Bangiophyceae) and salmon cages for reduced environmental impact and

increased economic output. Aquaculture 156:45–61.

Troell, M., P. Ronnback, C. Halling, N. Kautsky and A.H. Buschmann. 1999.

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nutrients from the intensive mariculture. J. Appl. Phycol., 11: 89-97.

 

 

 

 

 

 

 

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Chapter 2: A Comparison of Nutrients Fluxes in Monoculture and

Polyculture Systems for Shrimp (Penaeus vannamei) and

Seaweed (Gracillaria verrucosa) Production

 

Y. N. Ihsanab, K. J. Hessec, N. Holmgrend, C. Schulzab

aGesellschaft für Marine Aquakultur mbH, Hafentörn 3, D-25761 Büsum

bInstitute for Animal Breeding and Husbandry, Christian-Albrechts-Universität

D-24098 Kiel

cResearch and Technology Centre, Christian-Albrechts-Universität

D-25761 Büsum

dUniversity of Skövde – Sweden

541 28, Skövde – Sweden

Submitted to the Journal of World Aquaculture Society

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Abstract

Integrated aquaculture systems are well known to utilize various forms of

nutrients with higher total assimilation rates than monoculture. In order to

evaluate the nutrient efficiency of combined shrimp and seaweed production

nutrient fluxes were compared with shrimp monoculture systems. Therefore

triplicate ponds of 1200 m² were stocked with Gracillaria verrucosa (50 kg) and

20 individuals of shrimp (0.22 ± 0.016 g/ind)/m2. The culture period lasted 100

days and water samples to describe nutrient fluxes were taken every 10 days. The

average ammonium-nitrogen concentration over the whole period was 0.24 mg/l

in polyculture while in monoculture 0.37 mg/l of ammonium-nitrogen were

analyzed. Survival rate of shrimp in polyculture and monoculture were 86.32%

and 69.17% respectively. A mass balance model was developed for total nitrogen

and total phosphorus to estimate their fluxes. From the total nitrogen and total

phosphorus input, 24.2% and 5.3% were incorporated in 335.7 kg/1200 m2 shrimp

weight gain in monoculture, while 30.8% and 6.9% were incorporated in 501.5

kg/1200m2 shrimp weight gain and 3.5% and 2.4% were incorporated in 325

kg/1200 m2 seaweed Gracillaria in polyculture system. Therefore, polyculture

systems using seaweed Gracillaria seem to act more efficiently with regard to

nutrient accumulation.

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Introduction

Shrimp aquaculture has been developed towards a commercial industry in

Southeast Asian countries including Indonesia. The coastal area, which includes

mangrove forests, has been changed to be utilized for aquaculture activities within

the last decades (Clough, 1993). Moreover, an effluent containing a large quantity

of nutrients as a result of feed and fertilizer application, has been discharged from

aquaculture ponds into the environment. Rapid development of intensive

aquaculture in coastal areas throughout the world has raised increasing concerns

on its environmental impact (Wu, 1995; Mazzola et al., 1999). Organic and

inorganic inputs have led to a substantial increase of nutrient loading in coastal

waters.

In general, shrimp culture produces a large amount of waste, including nitrogen

and phosphorus, that is released to the aquatic environment. Feed and fertilizer

which are applied in shrimp ponds are not fully incorporated into the shrimp, but

partly deposited in pond sediments or discharged as effluents. In average, shrimp

assimilates only 23-31% of nitrogen and 10-13% of phosphorus of the total

inputs. While remaining 14-53% of nitrogen inputs and 39-67% of phosphorus

inputs are deposited in the sediment (Dhirendra and Lin, 2002). Nutrient in

aquaculture effluents are distributed in a particulate or soluble fraction (Ackefors

and Enell, 1994). In fresh manure, about 7-32% of total nitrogen (TN) and 30-

84% of total phosphorus (TP) are bound in this particulate fraction and the

remainder are excreted in dissolved forms (Bergheim et al., 1993). In intensive

marine shrimp culture, only 24% and 13% of dietary nitrogen and phosphorus

were incorporated into harvested shrimp, while the remaining nutrients were

released into the surrounding water (Briggs and Funge-Smith, 1994). Phosphorus

releases were estimated to be 9.4 kg (Ackefors and Enell, 1990) and 19.6–22.4 kg

(Holby and Hall, 1991) per tonne of shrimp produced.

The nutrient releases during pond draining at harvest were exceeding or equaling

the limitations recommended by the U.S. Environment Protection Agency (Choo

and Tanaka, 2000). On the other hand, tidal mangrove estuaries impacted by

shrimp pond effluent, have some capacity to process intermittent inputs of pond-

derived nutrients. Mangrove vegetation is capable of removing excessive

  22

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nutrients, of up to 70% of nutrient input for NO3--N and NH4

+-N, reducing PO42--

P fluctuation, and producing bioactive compounds (Primavera, 2000).

In recent years, there has been increasing emphasis on developing treatment

systems for aquacultural effluents. Schulz et al. (2003) reported the total

suspended solids (TSS) were reduced by 95.8-97.3% from rainbow trout farm

effluent in constructed wetland with emergent plants and subsurface horizontal

water flow. This nutrient incorporation of co-cultured organisms of different

trophic levels is the basis of environmentally sounded aquaculture (Chopin et al.,

2001; Neori et al., 2004). Ideally, nutrient process in polyculture system with two

or more ecologically compatible species should be balanced, waste from one

species are recycled as fertilizer or feed by another without conflicting with each

other (Neori et al., 2000). By integrating fed mariculture (fish and shrimp) with

extractive mariculture (seaweed), the wastes of one resource consumer become a

source (fertilizer or feed) for others in the system. Such a balanced ecosystem

approach provides nutrient bioremediation capacity, mutual benefits to co-

cultured organisms, and economic diversification by producing other value added

materials (Chopin et al., 2001).

Silvofisheries or aquasilviculture, in which low-density cultures are integrated in

mangrove areas, have been reviewed by Primavera (2000). Mangrove ecosystem

plays an obvious role in maintaining the biological balance in the coastal

environment where shrimp ponds are usually constructed. The removal of

mangroves around shrimp ponds has frequently resulted in harvest failure. Boyd

(1999) claimed that mangrove forests are not a suitable site for shrimp farms due

to many reasons such as inadequate slope for drainage, excessive organic matter

releases, nitrogen, phosphorus, acid sulphate soil or pyrite discharge. Effluent

treatment in shrimp aquaculture by macroalgae co-cultivation is still not generally

practiced. However, studies investigating the performance of integrated

mariculture (polyculture) in open-waters, have been hampered by the difficulties

involved with the experimental setup and data collection at sea (Petrell and Alie,

1996; Troell et al., 1997; Neori, 2004).

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In this research, we aim to compare nutrient fluxes in shrimp monoculture with

shrimps and seaweed polyculture systems designed to enhance nutrient utilization

and to decrease environmental impact of aquaculture activities.

Materials and methods

This study was conducted at the Sungai Buntu research station, Research Institute

for Brackish water fisheries, West Java, Indonesia (Figure 1). Shrimp aquaculture

was intensively carried out for about 3 months from 26 September 2009 to 05

Januar 2010. The experimental site was divided into 3 divisions: Water input

(canal) approximately 1 ha, triplicate of shrimp aquaculture ponds (intensive

monoculture) and triplicate of shrimp + seaweed Gracillaria ponds (intensive

polyculture) (Figure 2). The area of each pond was 1200 m2 (40 m x 30 m) and

the water depth of each pond was 1 m.

Location of experiments

(Sungai Buntu-West Java)

Figure 1. Map of Research Institute for Brackish water fisheries, West Java,

Indonesia

  24

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Sampling point:A. Water inflowB. Polyculture systemC. Monoculture system

: Gracilaria

Figure 2. Schematic outline of shrimp monoculture and polyculture systems

Each pond was fertilized with 3 kg of urea before stocking of shrimp and

Gracillaria. Fertilizers were used to increase primary productivity or natural food

establishment in ponds.

The seaweed Gracillaria (Gracillaria verrucosa), provided from local production

in Sungai Buntu, Karawang-West Java was inserted into polyethylene ropes that

were fixed by the rafts. A suspension culture unit was composed of four rafts,

each in turn of nine ropes. Each rope (about 10 m long) was inserted with a piece

of alga (15 g) every 20 cm. Distance between adjacent ropes was 50 cm and

between adjacent units distance was 3 m.

Shrimp Penaeus vannamei post larvae (0.22 ± 0.016 g/ind) were stocked at a

density of 20 individuals/m2 (Table 2) in each of the 6 ponds. Triplicate

polyculture ponds of 1200 m² were additionally stocked with Gracillaria. Before

stocking, shrimp were acclimatized for one night to the pond water conditions.

Control sampling of shrimp weight gain was realized every 10 days to determine

the actual weight for feed application. 5 individuals were taken to be weighed.

Feed supplied equaled to 7-10% of shrimp biomass in accordance to time after

control sampling (modified after Baliao and Tookwinas, 2002). At day 0 and day

1 after sampling, daily feed supply amounted 7%, from day 2 until day 4 8%,

from day 5 until day 7 9% and from day 8 until day 9 10%. Feed was given 4

Ocean (North Java Sea)

Fresh sea water input

Water Stock

Chanel

River

Water input

Waste water output

Intensive polyculturesystem

Intensive monocilturesystem

A

B B B

C C C

Ocean (North Java Sea)

Fresh sea water input Chanel

River Waste water output

Intensive polyculturesystem

Intensive monocilturesystem

A

B B B

C C C

Sampling point:A. Water inflowB. Polyculture systemC. Monoculture system

: Gracilaria

Ocean (North Java Sea)

Fresh sea water input

Water Stock

Chanel

River

Ocean (North Java Sea)

Water input

Waste water output

Intensive polyculturesystem

Intensive monocilturesystem

A

B B B

C C C

Fresh sea water input Chanel

River Waste water output

Intensive polyculturesystem

A

B B B

C C C

Intensive monocilturesystem

  25

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times a day, i.e. at 07.00, 12.00, 17.00 and 22.00. Two percent of the water

volume of the shrimp ponds was added every day.

Every 10 days ponds were monitored to estimate the survival rate (SR) of shrimp.

Survival rate (SR) was calculated as ratio between the numbers of shrimp at a

certain time (at sampling) to the number of shrimp at the time of stocking. To

determine the number of shrimp at sampling following formula were used:

Nt = Nu * Lt / Lj

Description:

Nt = number of shrimp in ponds at time-t

Nu = number of shrimp caught in nets at each sampling time-t

Lt = pond area (m2)

Lj = net effective aperture area (m2).

Nutrient sampling

Every 10 days, the water quality (ammonium-nitrogen, nitrate-nitrogen, nitrite-

nitrogen, orthophosphate-phosphorus and hydrogen sulphide) were analysed. The

samples were taken over 24 hours by intervals of 3 hours. Water sample were

taken 20 cm below the water surface. Every day at 08.00 and 16.00, water

temperature, salinity, and dissolved oxygen (DO) were monitored in situ with a

portable water quality sensor system (TOA model WQC-20A electronic Ltd.,

Japan). Water samples were collected using plastic bottles installed at the edge of

a stick. They were immediately filtered through Whatman GF/F filters 0.7 µM

millipore for soluble nutrients analyses (PO4-3, NO3

-, NO2_, NH4

+). The

ammonium-nitrogen concentration in the filtrate was measured immediately after

filtration. Total nitrogen (TN), total phosphorus (TP), nitrate-nitrogen, nitrite-

nitrogen, and orthophosphat concentrations were measured by the APHA (1995)

standard method. The nutrient analyses were performed by spectrophotometer

(Shimadzu UV-2400).

The standard methods for the determination of ammonium-, nitrite- and nitrate-

nitrogen were based on moderate alkaline solution with hypochlorite,

diazotization and cadmium reduction followed by diazotization, respectively. The

standard method for the determination of orthophosphat was based on the reaction

  26

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of the phosphorus ions with an acidified molybdate reagent. The

spectrophotometer wave length for ammonium-nitrogen, nitrite-nitrogen, nitrate-

nitrogen and phosphorus were 630 nm, 542 nm, 542 nm and 882 nm, respectively.

Pre-ashed (500 °C) and weight of GF/F filters in glass dishes were used to

determine suspended solids in accordance to standard filtration method

(APHA,1995). Nitrogen and phosporus content in organic matter of shrimp feed,

shrimp, Gracillaria and total suspended solids were measured using Kjehdahl

method. H2S was measured by Cline methode based on N, N-dimethyl-p-

phenylenediamine (Cline, 1968).

Statistics

Water quality and nutrient fluxes from water inflow, monoculture and polyculture

ponds were analyzed statistically. All data were checked for normality

(Kolmogorov – Smirnov test) and homogeneity of variances (HOV, Brown

Forsythe test). Differences of means of triplicate ponds (n=3) were evaluated for

significance by the range tests of Tukey HSD (P<0.05) for homogeneous variance

and for inhomogeneous variances Dunnett-T-3 test was used. Calculations were

performed with the SPSS software package (SPSS, 1999).

Mass balance

Considering the gross nutrient mass balance, the environmental losses of TN (LN)

or TP (LP) can be explained by equation below:

LN = (FCN + fCN + ICN + SSCN + SGCN) – (HSCN + HGCN + OCN)

LP = (FCP + fCP + ICP + SSCP + SGCP) – (HSCP + HGCP + OCP)

FC : Content of N or P in dry pellet

fC : Content of N or P in fertilizer

IC : Content of N or P in in flowing water

SSC : Content of N or P in stocked shrimp

SGC : Content of N or P in stocked Gracillaria

HSC : Content of N or P in harvested shrimp

HGC : Content of N or P in harvested Gracillaria

OC : Content of N or P in out flowing water

  27

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Result and discussion

Water quality

Water temperature ranged from 23.7–28.7 ºC. Average values of temperature

ranged between 26.5–27.8 oC at sampling points. Salinity also showed no

significant difference between the mono- and polyculture systems (P>0.05).

Average values of salinity for inflow water (canal), monoculture and polyculture

ponds were 36.7 ppt, 38.2 ppt and 37.7 ppt, respectively (Table 1). This values

were high as the experiments were realized during dry season. Dissolved oxygen

in water is the most important factor which determines water quality for

aquacultural purposes. Appropriate dissolved oxygen (DO) level for shrimp

aquaculture are higher than 3 mg/l. In this study, the average of dissolved oxygen

(DO) over 100 days period in monoculture was 3.03 mg/l while in polyculture

significantly higher DO values of 4.77 mg/l were recorded (Tabel 1). It can be

assumed that in day light, Gracillaria produces sufficient amounts of oxygen by

photosynthesis activities.

Table 1. Water quality parameter over 100 days period

Parameter Inflow Monoculture Polyculture

Temperature (oC) 27.84a 26.5±1.02 a 26.50±1.05 a

Dissolved oxygen (mg/l) 4.2 a 3.03±0.58 b 4.77±0.67 a

Salinity (ppt) 36.7 a 38.18±0.74 a 37.72±0.57 a

pH 7.75 a 7.77±0.15 a 7.73±0.17 a

TSS (mg/l)* 15.6 a 59.89±8.44 b 56.5±7.53 b

TN (mg/l)* 0.95 a 2.97±0.50 b 3.2±0.33 b

TP (mg/l)* 0.17 a 1.3±0.19 b 1.1±0.22 b

NH4+-N (mg/l) 0.014 a 0.37±0.04 b 0.24±0.03 c

NO3--N (mg/l) 0.004 a 0.018±0.001 b 0.017±0.001b

NO2--N (mg/l) 0.0002a 0.002±0.0005b 0.002±0.0004b

PO4-P (mg/l) 0.001a 0.005±0.0006b 0.004±0.0008b

Values given are means of 10 times sampling in triplicate ponds. (*TSS, TN, and TP are

means of 4 times sampling in triplicate ponds).

Values with the same superscript letter do not differ significantly (P>0.05).

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Xu (2008) reported the Gracillaria cultivation can improve other aspects of water

quality instead of increasing DO. Its photosynthesis produces DO that promotes

decomposition of organics. Density raft culture of Gracillaria impedes the water

circulation and may decrease chemical oxygen demand (COD) in the water

column. In addition, several species of Gracillaria can produce oxygen under low

light condition, such as in rainy days and remediate anoxia (Xu et al., 2004).

00.0020.0040.0060.0080.01

0.0120.0140.0160.0180.02

0 20 40 60 80 100 120

Time (days)

Conc

entra

tion

(mg/

l)

PolycultureMonocultureInflow

a

b

c

a

a

cc

a

a

a

b

c

 

Figure 3. Concentration of H2S during the experimental period, values are

mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05).

Hydrogen sulfide (H2S) can severely affect shrimp growth in pond. H2S is

produced by chemical reduction of organic matter that accumulates and forms a

thick layer of organic deposits at the bottom. High levels of hydrogen sulfide

would affect directly demersal or burrowing shrimps such as Peneaus monodon.

At levels of 0.1–0.2 mg/l of H2S in the water, shrimp growth will be disturbed and

die instantly at concentration higher than 4 mg/l (Law, 1988). In this study,

hydrogen sulfide (H2S) presented after 60 days. Highest hydrogen sulfide (H2S)

levels of 0.018 mg/l were recorded at harvest for the monoculture system and of

  29

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0.009 mg/l for the polyculture system (figure 3). This means that H2S was not

harmful for the growth of shrimp in monoculture and polyculture system.

Nutrients fluxes

Dissolved nutrient fixation is one of the core advantages of constructed wetlands

compared to standard mechanical effluent treatment (Schulz, 2003). In this study,

the ammonium concentration increased gradually in monoculture and polyculture

systems and orthophosphate concentration progressively increased as well.

Though well water was supplied to the pond, the ammonium-nitrogen

concentrations in monoculture increased from 0.005 to 0.779 mg/l (Figure 4), with

an average concentration of ammonium-nitrogen during the 100 days period of

0.37 mg/l (Table 1). In polyculture system, it increased from 0.003 to 0.483 mg/l

(Figure 4), with an average of 0.24 mg/l. Therefore, ammonium-nitrogen

concentrations were significantly higher in comparison to polyculture system

(P<0.05), in which Gracillaria assimilated ammonium from water.

00.10.20.30.40.50.60.70.80.9

0 20 40 60 80 100 120

Time (days)

Conc

entr

atio

n (m

g/l) Monoculture

PolycultureInflowa a

aa

a a

b b bb b b

c c c c c ca ac

 

Figure 4. Concentration of ammonium-nitrogen (NH4--N) during the

experimental period, values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05).

  30

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00.0050.01

0.0150.02

0.0250.03

0.0350.04

0.045

0 20 40 60 80 100 120

Time (days)

Conc

entr

atio

n (m

g/l)

MonoculturePolycultureInflow

b b b b b bb

bb

b

aa

a aa

a

a

a

a

a

aa

a a a

aa

aa

a

 

Figure 5. Concentrations of nitrate-nitrogen (NO3+-N) during the

experimental period, values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05).

00.0010.0020.0030.0040.0050.0060.0070.008

0 20 40 60 80 100 120

Time (days)

Conc

entra

tion

(mg/

l)

MonoculturepolycultureInflow

aa

a

a

a

a

aa

a

a

a b b b b b b b aa

a

a

a a

a

aa

 

Figure 6. Concentrations of nitrite-nitrogen (NO2+-N) during the

experimental period, values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05).

Low values of nitrate- and nitrite-nitrogen, of 0.0044 and 0.0002 mg/l (Table 1)

were observed in the pond inlet and higher values were generated, possibly by

nitrification bacteria in the pond systems. Nevertheless, no differences could be

  31

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observed for nitrate and nitrite in monoculture or polyculture systems during the

experiment (P>0.05) (Figures 5 and 6). The average concentration of nitrate and

nitrite-nitrogen in the monoculture system were 0.018 and 0.002 mg/l,

respectively, and 0.017 and 0.002 mg/l in polyculture system (Table 1).

Hopkins et al. (1995) found that particulate matter and dissolved nutrients in the

outflow water increased considerably with higher water exchange rates. The

authors concluded that assimilation by phytoplankton and nitrifying bacteria

attached to detritus particles are the main processes of nitrogen removal from the

water column Hargreaves (1998) suggests that the potential for N removal from

ponds by denitrification is high.

0123456789

0 20 40 60 80 100 120

Time (days)

Conc

entra

tion

(mg/

l)

PolycultureMonocultureInflow

aa

b

a

a

a

a

bb

 

Figure 7. Concentrations of Total Nitrogen (TN) during the experimental

period, values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05).

  32

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0

0.002

0.004

0.006

0.008

0.01

0 20 40 60 80 100 120

Time (days)

conc

entra

tion

(mg/

l)

MonoculturePolycultureInflow

a

aa a a a

a a a a

ab

b

b

b b

ab

aa

a a aa

b b

bb b b

 

Figure 8. Concentration of Orthophosphate (PO4) during the experimental

period, values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05).

-0.50

0.51

1.52

2.53

3.5

0 20 40 60 80 100 120

Time (days)

Conc

entra

tion

(mg/

l)

PolycultureMonocultureInflow

a

a

a

a

a

a

bb b

 

Figure 9. Concentrations of Total Phosphorus (TP) during the experimental

period, values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05).

  33

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Total nitrogen (TN) and total phosphorus (TP) concentration increased in the

outlet water of polyculture and monoculture ponds. TN in polyculture ponds

increased from 0.15-7.43 mg/l (Figure 7), with an average of 3.2 mg/l (Table 1),

while in monoculture TN ranged from 0.13–7.26 mg/l (Figure 7), with an average

of 2.97 mg/l (Table 1). TP in polyculture pond increased from 0.015–2.83 mg/l

(Figure 9), with an average of 1.1 mg/l (Table 1), while in monoculture values of

0.013–2.41 mg/l (Figure 9) and an average of 1.3 mg/l (Table 1) could be

observed, but no significant differences (P>0.05) could be observed between the

systems.

The average concentrations of orthophosphate in the inlet water, monoculture and

polyculture effluents during the 100 days period were 0.001, 0.005 and 0.004

mg/l, respectively (Table 1). There were no significant differences between

monoculture and polyculture system (P>0.05). Orthophosphate increased from

0.0012 mg/l to 0.0081 mg/l for monoculture and 0.0012 mg/l to 0.0067 mg/l for

the polyculture systems (Figure 8). It can be assumed that the initial concentration

of phosphorus was not influenced by inflowing phosphorus.

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Table 2. Performance of experimental intensive shrimp polyculture and

monoculture system over 100 days period (n=3)

Parameter Polyculture Monoculture

Stocked larvae:

Stocking density

(Individuals/m2)

Total larvae (ind)

Weight (g/ind)

Total weight (kg)

20

24000

0.22 ± 0.016

5.1

20

24000

0.22 ± 0.016

5.1

Culture time (days) 100 100

At harvest:

Shrimp (ind/ m2)

Total shrimp

Individual weight

(g/ind)

Weight (kg/m2)

Total weight (kg)

16.8 a

20141 a

24.9 ± 1.8 a

0.42

501.5

13.5 b

16140 b

20.8 ± 1.05 b

0.28

335.7

Survival rate (%) 86.32 a 69.17 b

Total Feed (kg) 826.7 a 620 b

FCR 1.67 a 1.88 b

Values with the same superscript letter do not differ significantly (P>0.05).

Seventy thousand post larvae (PL) were stocked in the triplicate ponds with a

density of 20 ind/m2. Initial weight of individual larvae (PL) was 0.22 ± 0.016 g

resulting in a total stocking weight of approximately 5.1 kg/1200 m2.

Approximately 826.7 kg/ of pelleted feed was supplied for each polyculture

system pond and 620 kg for the triplicate monoculture ponds (Table 2). 501.5

kg/1200 m2 of shrimp were harvested for the polyculture system and 335.7

kg/1200 m2 for the monoculture system (Table 2). Feed given to the polyculture

ponds was higher compared to the monoculture shrimp due to the higher growth

performance in polyculture ponds. The average final weight of shrimp was 24.9 ±

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1.8 g for polyculture systems with survival rates of 86.3%. For monoculture, the

weight of shrimp was 20.8 ± 1.05 g and survival rate accounted 69.17% (Table 2).

Survival rate of shrimp in polyculture was significantly higher than in

monoculture, and the weight of shrimp as well (P<0.05). The feed conversion

ratio (FCR) for the polyculture and monoculture system in this study were 1.67

and 1.88, respectively (Table 2) and they were significantly different (P<0.05). In

comparison to global average shrimp feed conversion ratio of around 2.0 observed

feed conversions was quite good (Tacon, 2002).

Results from this study showed clear differences in performance parameters

between monoculture and polyculture system. Shrimp growth and production

were reported to be basically related to stocking density, feeding management and

water quality (Songsangjinda, 1994). In addition, cited experiment did not make

any note about serious diseases outbreak in monoculture. This result may indicate

that seaweed Gracillaria play a vital role on system productivity. Several reports

have shown that enrichment of aquaculture ponds with nutrients changes both

quality and quantity of nitrogen and phosphorus compounds in the water column,

resulting in varying phytoplankton community in the ponds (Alonso-Rodriguez

and Paez-Osuna. 2003). The ability of Gracillaria verrucosa as a biofilter showed

by its ability to absorb nutrients that are not needed by the shrimp (Figures 10 and

11). Therefore, this residual feed was not turn into toxic substances. That means

the environmental conditions for growth of shrimp in polyculture system is better

than monoculture. Apart from removing nutrients, the seaweed Gracillaria may

contribute to the oxygen budget of the ponds.

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Mass balance

Mass Balance calculations for nutrients are important to evaluate the efficiency of

feed nutrient utilization in order to estimate the polluting potential of pond

effluents (Tucker and Boyd, 1985; Briggs and Simon, 1994).

TN-mass balance polyculture system 

Outlet water 21.3%

(11.27 kg)a

Water inflow 6.9%

(3.65 kg)

Pond WaterFertilization 3% (1.56 kg)

Shrimp feed 90%

(47.6 kg)a

Shrimp harvest 30.8% (16.27 kg)a Seaweed harvest

3.5% (1.83 kg)

Stocked shrimp0.06%(0.03 kg)

Seaweed stocked0.04%(0.02 kg)

Others associated44.4%(23.49 kg)

Outlet water 21.3%

(11.27 kg)a

Water inflow 6.9%

(3.65 kg)

Pond WaterFertilization 3% (1.56 kg)

Shrimp feed 90%

(47.6 kg)a

Shrimp harvest 30.8% (16.27 kg)a Seaweed harvest

3.5% (1.83 kg)

Stocked shrimp0.06%(0.03 kg)

Seaweed stocked0.04%(0.02 kg)

Others associated44.4%(23.49 kg)

 

TN-mass balance monoculture system

Outlet water 25.4%

(10.4 kg)a

Pond Water

Water inflow 8.9% (3.65 kg)

Fertilization 3.8% (1.56 kg)

Shrimp food 87.2% (35.73 kg)b

Shrimp harvest 24.2% (9.9 kg)b

Shrimp stocked<0.1%(<0.03 kg)

Others Associated50.4%(20.67 kg)

Outlet water 25.4%

(10.4 kg)a

Pond Water

Water inflow 8.9% (3.65 kg)

Fertilization 3.8% (1.56 kg)

Shrimp food 87.2% (35.73 kg)b

Shrimp harvest 24.2% (9.9 kg)b

Shrimp stocked<0.1%(<0.03 kg)

Others Associated50.4%(20.67 kg)

 

Figure 10. Total nitrogen mass balance in experimental polyculture and

monoculture systems. Values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly between mono- and

polyculture systems (P>0.05).

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TP-mass balance polyculture system 

Pond Water

Water inflow 6.2% (0.6)

Fertilization 2% (0.2 kg)

Shrimp food 91.74% (8.9 kg)a

Shrimp harvest 6.9% (0.67 kg)a

Seaweed harvest 2.4%

(0.23 kg)

Outlet water 47.3% (4.6 kg)a

Shrimp stocked0.2%(0.02 kg)

Seaweed Stocked0.06%(0.006 kg)

OthersAssociated43.4%(4.23 kg)

Pond Water

Water inflow 6.2% (0.6)

Fertilization 2% (0.2 kg)

Shrimp food 91.74% (8.9 kg)a

Shrimp harvest 6.9% (0.67 kg)a

Seaweed harvest 2.4%

(0.23 kg)

Outlet water 47.3% (4.6 kg)a

Shrimp stocked0.2%(0.02 kg)

Seaweed Stocked0.06%(0.006 kg)

OthersAssociated43.4%(4.23 kg)

 

TP-mass balance monoculture system

Outlet water 51.9% (3.9 kg)a

Water inflow 7.9% (0.6 kg)

Pond Water

Fertilization 2.7% (0.2 kg)

Shrimp food 89.1% (6.7 kg)b

Shrimp harvest 5.3% (0.4 kg)b

Shrimp stocked0.3%(0.02 kg)

Others Associated42.8%(3.22 kg)

Outlet water 51.9% (3.9 kg)a

Water inflow 7.9% (0.6 kg)

Pond Water

Fertilization 2.7% (0.2 kg)

Shrimp food 89.1% (6.7 kg)b

Shrimp harvest 5.3% (0.4 kg)b

Shrimp stocked0.3%(0.02 kg)

Others Associated42.8%(3.22 kg)

 

Figure 11. Total phosphate mass balance in experimental polyculture and

monoculture systems. Values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly between mono- and

polyculture systems (P>0.05).

  38

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Using the strategy proposed by Funge-Smith and Briggs (1998), a mass balance

for the fate of nutrients in feed added to shrimp ponds was developed based on the

nutrient amount of feed and fertilizer added, shrimp and Gracillaria stocked,

shrimp and Gracillaria harvested, and nutrients in and out-flowing water.

Each pond was fertilized with approximately 3 kg urea/1200 m2 before stocking.

Total nitrogen (TN) and total phosphate (TP) from fertilizer were 1.56 kg/1200 m2

and 0.2 kg/1200 m2 for the monoculture and polyculture system. Whereas TN and

TP from inflowing water were 3.65 kg/1200 m2 and 0.6 kg/1200 m2 for the

monoculture and polyculture system (Figures 10 and 11). Outlet water contained

10.4 kg/1200 m2 and 3.9 kg/1200 m2 of total nitrogen (TN) and total phosphorus

(TP), for the monoculture system and 11.27 kg/1200 m2 and 4.6 kg for the

polyculture system (Figures 10 and 11). 

Figure 10 and 11 showed total nitrogen and total phosphorus mass balance in

polyculture system with a growth performance of 0.42 kg shrimp m-2 and 0.3 kg

Gracillaria m-2 and a feed conversion ratio of 1.67 (shrimp: 34.5% dry matter,

9.4% N, 0.38% P; Feed: 90% dry matter) and with 0.28 kg shrimp m-2 and a feed

conversion ratio of 1.88 (shrimp: 33% dry matter, 8.9% N, 0.3% P; Feed: 90% dry

matter) in monoculture system.

In addition, monoculture system were characterised by 8.9% and 0.3% of applied

total nitrogen (TN) and total phosphorus (TP) incorporated in shrimp and 9.4%

and 0.38% in shrimps of the polyculture system. Gracillaria incorporated 3.31%

and 0.42% of total nitrogen (TN) and total phosphorus (TP) in polyculture

system. When shrimp were harvested, at least about 24.2% of the total nitrogen

(TN) and 5.3% of the total phosphorus (TP) for the monoculture system and about

34.3% (30.8% from shrimp harvest and 3.5% from seaweed harvest) of the total

nitrogen (TN) and 9.3% (6.9% from shrimp harvest and 2.4% from seaweed

harvest) of the total phosphorus (TP) for the polyculture system were removed

(Figures 10 and 11). Total nitrogen and total phosphorus in outlet water amounted

10.4 kg/1200 m2 and 3.9 kg/1200 m2 in the monoculture system. In the

polyculture ponds 11.27 kg/1200 m2 and 4.6 kg/1200 m2 of TP and TN were

recorded in outlet water (Figures 10 and 11).

  39

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The largest source of nitrogen originated from feed with 87.2% for the

monoculture and 90% for the polyculture system. The remaining nitrogen derived

from fertilizer and inflowing water, 3.8% and 8.9% for the monoculture and 3%

and 6.9% for the polyculture system (Figure 10). Outlet water contained 25.4% of

total nitrogen for the monoculture and 21.3% for the polyculture system (Figure

10). Denitrification, ammonium volatilization and total nitrogen in other organism

e.g. benthos and zooplankton were not directly evaluated in this study, but 50.4%

of total nitrogen input for the monoculture and 44.4% for the polyculture system

could be analyzed as unidentified losses. This loss of nitrogen was assumed to be

lost to the atmosphere as N2 via denitrification. The volatilization of nitrogen

emphasizes the significance of microbial decomposition process in ponds.

Another possibility for this loss of nitrogen could be the incorporation into other

organisms. Hopkins et al. (1993) could not account for 13 - 46% of total nitrogen

input in intensive shrimp ponds. 27.4% of the total nitrogen was unaccounted in a

semi intensive shrimp farm in North-Western Mexico explained by denitrification

and atmospheric diffusion of unionized ammonia (Paez-Osuna et al. 1997).

N-fixation by blue-green algae was not taken into account by the model, and the

significance of this contribution is unknown. In this model, the amount of nitrogen

from stocking larvae and Gracillaria were only 0.03 kg/1200 m2 and 0.02

kg/1200 m2 respectively.

The nitrogen mass balance reveal in detail, the source and sink of the organic

component in a shrimp pond. Funge-Smith and Briggs (1998) reported the actual

amount of nutrients assimilated into shrimp biomass is a small fraction of the total

amount applied as feed. Only 18-27% of nitrogen applied to the pond was

assimilated into shrimp, thus there is considerable wastage as nutrients are

incorporated into plankton biomass, volatilized or trapped in the sediment. The

sinks for nitrogen are the sediments (24%), harvested shrimp (18-27%) and

discharge water (27%). Approximately 30% of the nitrogen unaccounted is

assumed to be N losses to the atmosphere as N2 or ammonia.

The largest source of total phosphorus (TP) originated from feed, 89.1 % for the

monoculture and 91.74% for the polyculture system. The rest of TP derived from

fertilizer and water input were 2.7% and 7.9% for the monoculture systems and

  40

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2% and 6.2% for the polyculture system, respectively (Figure 11). Total

phosphorus in outlet water was 51.9% in the monoculture and 47.3% in the

polyculture system of total phosphorus input (Figure 11). That means, 51.9% of

total phosphorus input for monoculture and 47.3% of total phosphorus input for

polyculture system were discharged to the environment. TP associated in other

organisms e.g. benthos and zooplankton was not directly evaluated in this study,

but 42.8% of total phosphorus input for the monoculture and 43.4% for the

polyculture system were unaccounted. It can be assumed that this amount is lost

through consumption by other macrofauna or fixed in minerals in sediment.

The processes of denitrification, ammonia volatilization and phosphorus

adsorption by sediments serve to regulate their concentrations in the water column

(Tucker and Boyd, 1985). Boyd (1985) reported that 56% of phosphorus inputs in

freshwater catfish ponds was lost through uptake by sediments. Briggs and Funge-

Smith (1994) reported that 84% of the phosphorus was retained in the sediments

of intensive marine shrimp ponds in Thailand. Funge-Smith and Briggs (1998)

reported the principal source of phosphorus in intensive shrimp ponds was the

applied feed (51%). The 26% shortfall in inputs was assumed to be the eroded

pond bottom. Effluent water constituted 10% of TP loss in the budget and this is

mainly bound in the suspended solid fraction. Thus, trapping of the suspended

solid fraction is important to minimize its environmental impact.

Effluents from shrimp aquaculture typically were enriched in suspended solid and

nutrients. Different alternatives have been considered to mitigate or resolve the

impact of shrimp pond effluents on the water quality of adjacent coastal waters.

The use of polyculture technology, with shrimp and seaweed, have been

positively evaluated in this study. Improved pond design, construction of buffer

ponds, reduction and elimination of water exchange rates are other interesting

alternatives that could reduce the impact of shrimp pond effluents (Paez-Osuna,

2000), but for marginal areas polyculture seems to be a viable way to increase

nutrient efficiencies in shrimp aquaculture.

  41

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Conclusions

The seaweed Gracillaria can be cultivated in polyculture with shrimp. This

macroalgae can not only serve as an effective biofilter for shrimp ponds but also

can increase shrimp productivity. The weight and survival rate of shrimp in

polyculture systems were higher than in monoculture. The nutrients fluxes

demonstrate a high efficiency in polyculture systems than in monoculture. The

polyculture using Gracillaria as co-cultivation may thus encourage future

polyculture systems to be adopted by farmers as an environmentally friendly way

of aquaculture.

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JPrimavera.pdf (Verified 4 Jan. 2006)

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effluents in constructed wetland with emergent plants and subsurface

horizontal water flow. Aquaculture. Elsevier. 217. 207-221.

Shnel, N., Y. Barak, T. Ezer, Z. Dafni, J. van Rijn. 2002. Design and performance

of a zero-discharge tilapia recirculating system. Aquacultural Engineering.

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SPSS. 1999. Statistic software package. Release 9.0.1 for MS Windows.

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shrimp aquaculture. Report prepared under the World Bank, NACA,

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environment, published by consortium. 69.

Tucker, C. S. and C. E. Boyd. 1985. Water quality. In Water Quality (Channel

Catfish Culture Ponds), ed. C. S. Tucker, 135-227. Development in

Aquaculture and Fisheries Science. Elsevier. Netherlands.

Wu, R. 1995. The environmental impact of marine fish culture: towards a

sustainable future. Marine pollution Bulletin. 31. 159-166.

Xu, Y. J., N. Z. Jiao, L. M. Qian. 2004. Nitrogen nutritional identities of

Gracillaria as bioindicators and restoral plants (in Chinese with English

abstract). Journal of Fishery Sciences of China. 11. 276-281.

Xu, Y. J., J. Fang, Q. Tang, J. Lin, G. Le. 2008. Improvement of water quality by

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Chapter 3: Nutrient Fluxes and Mass Balances in Various

Polyculture Systems Using Shrimp (Penaeus vannamei), Fish

(Oreochromis sp.) and Seaweed (Gracillaria verrucosa)

Y. N. Ihsanab, K. J. Hessec, C. Schulzab

aGesellschaft für Marine Aquakultur mbH, Hafentörn 3, D-25761 Büsum

bInstitute for Animal Breeding and Husbandry, Christian-Albrechts-Universität

D-24098 Kiel

cResearch and Technology Centre, Christian-Albrechts-Universität

D-25761 Büsum

Submitted to the Journal of World Aquaculture Society

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Abstract

A comparative study on polyculture systems using various combinations of

shrimp (Penaeus vannamei), seaweed Gracillaria (Gracillaria verrucosa), and

fish (Oreochromis sp.) was conducted in order to calculate nutrients fluxes and

mass balances. Therefore, triplicate ponds of 1000 m2 size were stocked with 0.4

kg/m2 seaweed and 15 shrimps/m2 (polyculture I), and triplicate ponds of size

1000 m2 were stocked with 0.4 kg/m2 seaweed, 15 shrimps/m2, and 0.25 fish/m2

(polyculture II). Every 10 days during the 90-day culture period, pooled 24h-

water samples were taken to describe nutrient fluxes in the ponds. Water quality

in both polyculture systems were within the physiological ranges for the shrimp,

with whole period average total suspended solids (TSS) concentrations of 50.5 ±

7.6 mg/l in polyculture I, while in polyculture II TSS was 64.9 ± 4.2 mg/l. The

average total nitrogen (TN) and total phosphorus (TP) amount in polyculture I

were 2.25 ± 0.4 mg/l and 0.84 ± 0.05 mg/l, respectively, while in polyculture II

TN and TP amounted 2.66 ± 0.8 mg/l and 0.89 ± 0.05 mg/l, respectively. A mass

balance model was developed for total nitrogen and total phosphorus to estimate

their fluxes. From total nitrogen and total phosphorus input, 46.79% and 14.99%

were incorporated in 313.08 kg/1000 m2 shrimp weight gain in polyculture system

I, while 41.47% and 13.47% were incorporated in 291.25 kg/1000m2 shrimp

weight gain and 13.64% and 5.09% were incorporated in 40.67 kg/1000 m2 fish

weight gain in polyculture system II. Cultivated seaweed could remove up to

10.56% of supplied TN and 9.75% of TP in polyculture I, while 10.94% of

supplied TN and 8.83% of TP were incorporated seaweed in polyculture II. TN

and TP released into environment in polyculture I amounted 17.6% and 36.23%,

respectively, and in polyculture II 20.6% and 37.41%, respectively. These results

suggest that no significant differences in shrimp performance between the two

polyculture systems could be observed, additional fish biomass production in

polyculture II proves the higher nutrient retention.

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Introduction

In recent years the contribution of fish to global diets has reached a record of

about 17 kg per capita on average, supplying over three billion people with at

least 15 percent of their total animal derived protein intake (FAO, 2010). Marine

aquaculture has been a rapidly growing industry, increasing from about 18.6

million tons in 2006 to 20.1 million tons in 2009 and these patterns are expected

to continue up to the year 2030 due to the increasing global demand and high

market value of aquaculture products (FAO, 2010).

There are many obstacles such as diseases, environmental degradation and lack of

management that fish and shrimp farmers in Southeast Asia have to overcome

(Primavera, 1998). This means there is an urgent need to develop and disseminate

aquaculture practices in an economical yet still environmental friendly manner

(Funge-Smith and Briggs, 1998). One of the main environmental issues from open

aquaculture systems is the direct discharge of significant nutrient loads into the

environment. Resulting waste accumulation generated by the aquatic animal

farming can be divided into two categories: solid wastes consisting of non-eaten

feed, faecal material, and soluble products which include ammonia, urine,

dissolved organic matter and carbon dioxide. In aquaculture effluents, about 7-

32% of total nitrogen (TN) and 30-84% of total phosphorus (TP) and up to 27%

of total carbon are bound in the particulate fraction and the remainder can be

found in dissolved form (Bergheim et al., 1993). Nutrient in farm wastes

originating from feed supply are of greatest concern due to their role in

eutrophication processes (Persson, 1991) and discharge should be minimized as

much as possible and viable.

In shrimp aquaculture, environmental conditions in terms of both quantity and

quality have increasingly become a limiting factor so that the production has

shown a tendency to shift from area-based cultivation (extensive) towards

intensified systems (Thakur and Lin, 2003). The excretion of remaining feed

components in intensive systems will have the potential to degradate

environmental conditions for shrimp culture (Boyd, 1991; Primavera, 1994). The

degradation could cause an oxygen deficiency which in turn leads to anaerobic

conditions. In anaerobic conditions, decomposition of organic material will

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produce toxic compounds, especially ammonia (NH3) and hydrogen sulfide (H2S)

and resulting in decreased shrimp performance (Boyd, 1991; Goddard, 1996).

One way to improve aquaculture production and reduce the negative

environmental impacts is to perform polyculture systems that involve organisms

of different trophic levels. Ideally, the nutrient fluxes in the polyculture system

should be balanced with two or more ecologically compatible species, that waste

from one species is recycled to become input (fertilizer or feed) for another

species without conflicting each other (Neori et al., 2000).

In a previous study a comparison of nutrient fluxes and mass balances between

monoculture and polyculture systems using shrimp and seaweed Gracillaria has

been investigated (Ihsan et al., submitted). Polyculture systems, using seaweed

and shrimp, act more efficiently with regard to nutrient accumulation and system

performance. However, nutrient retention is often limited by additional needed

cultivation area, especially if plants are utilized (Buschmann et al., 2001). Thus,

polyculture systems using shrimp and seaweed in combination with omnivorous

tilapia proposed as a technological alternative for integrated aquaculture. At

present, this study focus on the calculation of nutrients fluxes and mass balances

in various polyculture systems using shrimp, seaweed and fish in order to identify

most efficient polyculture practices.

Material and method

The experiment was conducted in Sungai Buntu, West Java over a 90-day period

from July–October 2010 during the dry season. This area is located on the

northern Java Island (Figure 1). The experimental site was divided into 3 sectors:

Water input unit of approximately 1 ha, triplicate polyculture I systems consisting

of ponds stocked with shrimp and seaweed and triplicate polyculture II systems

consisting of shrimp + fish + seaweed ponds (Figure 2). The area of each pond

was 1000 m2 (40 m x 25 m). The water depth of each pond amounted 1 m. Each

pond was fertilized with 3 kg/1000 m2 of urea before stocking. Fertilizers were

used to activate and increase primary production and establishment of natural

feeds in ponds.

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Location of experiments (Sungai Buntu-West Java)Location of experiments (Sungai Buntu-West Java)

 

Figure 1. Map of Research Institute for Brackish water fisheries, West Java,

Indonesia

Figure 2. Schematic outline of polyculture systems I and II

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The seaweed, provided from local production in Sungai Buntu, Karawang, West

Java was inserted into polyethylene ropes that were fixed by rafts. A suspension

culture unit was composed of four rafts, with each in turn consisted of nine ropes.

Each rope (about 8.5 m long) was inserted with a piece of algae (25 g) every 20

cm. The distance between adjacent ropes and units was 20 cm 3 m, respectively.

Shrimp post larvae (0.43 ± 0.11 g) were stocked in each of the 6 ponds at a density

of 15 individuals/m2 and seaweed at a density of 0.4 kg/m2 (Table 2). Triplicate

polyculture II ponds of 1000 m² were additionally stocked with fish (4.7 ± 0.6

g/ind) at a density of 0.25 individuals/m2. Before stocking, shrimp and fish were

acclimatized for one night to the pond-water conditions.

Commercial shrimp feed (Luxindo 39, Luxindo Internusa Ltd.) containing 40%

protein was given. Control sampling of shrimp weight gain was done every 10

days to determine the actual weight for feed application. For this procedure 5

individuals were caught and analyzed. Daily feed supply equaled to 7-10% of

shrimp biomass in accordance to time after control sampling (modified after

Baliao and Tookwinas, 2002). At day 0 and day 1 after sampling, daily feed

supply amounted 7%/shrimp biomass, from day 2 until day 4 8%, from day 5 until

day 7 9% and from day 8 until day 9 10% shrimp biomass were fed. Feed was

given 4 times a day, i.e. at 07.00, 12.00, 17.00 and 22.00. Two percent of the

water volume of the shrimp ponds was exchanged every day.

Sampling and analytical procedures

Fluxes of following water quality parameters were measured: temperature,

salinity, dissolved oxygen (DO), pH, alkalinity, hydrogen sulphide (H2S), total

suspended solids (TSS), ammonium, nitrate, nitrite, orthophosphate, total nitrogen

(TN) and total phosphorus (TP).

Every 10 days, the water quality was analyzed. Samples of each pond sampling

point were taken over 24 hours at 3-hour intervals and pooled for following

analytical procedures. Water sample were taken 20 cm below the water surface in

central pond inlet and each pond outlet. Every day at 08.00 and 16.00, the water

temperature, salinity, and dissolved oxygen (DO) were monitored in situ using a

portable (TOA model WQC-20A Electronic Ltd., Japan) water-quality analyzer.

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Water samples were collected using plastic bottles attached to the end of a stick.

They were immediately filtered through Whatman GF/F filters 0.7 µM millipore

for soluble nutrients analyses (PO4-3, NO3

-, NO2_, NH4

+). The ammonium

concentration in the filtrate was measured immediately after filtration. Total

nitrogen (TN), total phosphorus (TP), nitrate, nitrite, and orthophosphate

concentrations were measured using the APHA (1995) standard methods. The

nutrient analyses were performed with a spectrophotometer (Shimadzu UV-2400).

The standard method for determining ammonium, nitrite and nitrate were based

on moderate alkaline solution with hypochlorite, diazotization, and cadmium

reduction followed by diazotization, respectively. The standard method for

determination of phosphorus in the water and feed and shrimp, seaweed or fish

samples was based on the reaction of ions with an acidified molybdate reagent.

The spectrophotometer wave lengths for ammonium, nitrite, nitrate and

phosphorus were 630 nm, 542 nm, 542 nm, and 882 nm, respectively. GF/F filters

in glass dishes were used to determine suspended solids. Total suspended solids

were estimated using the standard filtration method (APHA, 1995). H2S was

measured using the Cline-method based on N, N-dimethyl-p-phenylenediamine

(Cline, 1968). The spectrophotometer wave length for H2S was 670 nm. Nitrogen

content in the feed, shrimp, fish and seaweed were using Kjeldahl method.

Calculation

The growth performance criteria of shrimp and fish including survival rate,

specific growth rate, and feed conversion ratio were calculated at the end of the

experiment.

Survival Rate (SR) was calculated as a ratio between the shrimp or fish quantity at

sampling times and stocking time using the formula:

SR = (Nt / N0) X 100%

With: SR = survival rate

N0 = number of shrimp or fish on day 0 (individual)

Nt = number of shrimp or fish on day t (individual)

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Specific growth rate of shrimp or fish (SGR) represents the relative increase in

daily weight during a certain time interval and were calculated with:

SGR = ((ln Wt - ln W0) / t) X 100%

With: SGR = Specific growth rate

W0 = weight of shrimp or fish on day-0 (g)

Wt = weight of shrimp or fish on day-t (g)

t = time of experiment (day)

Feed conversion ratio (FCR) is the ratio between the amount of feed given to

shrimp weight gain in a certain period (NRC, 1977) using the formula:

FCR = F / ΔB

With: FCR = feed conversion ratio

F = amount of feed given during experiment (kg)

ΔB = shrimp biomass weight gain during experiment (kg)

Statistics

Water quality and nutrient fluxes and growth performance parameter observed

between polyculture I and polyculture II ponds were analyzed statistically. All

data were checked for normality (Kolmogorov-Smirnov test) and homogeneity of

variances (HOV, Brown-Forsythe test). Differences of means of triplicate ponds

(n=3) were evaluated for significance using the range tests of Tukey HSD

(P<0.05); for homogeneous variance and for inhomogeneous variances the

Dunnett-T-3 test was used. Calculations were made using the SPSS software

package (SPSS, 1999).

Mass balance

Considering the gross nutrient mass balance, the environmental losses of TN (LN)

or TP (LP) can be explained by following equation:

LN = (FCN + fCN + ICN + SSCN + SGCN + SFCN) – (HSCN + HGCN + HFCN +

OCN)

LP = (FCP + fCP + ICP + SSCP + SGCP + SFCp) – (HSCP + HGCP + HFCp +

OCP)

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FC : Content of N or P in dry pellet

fC : Content of N or P in fertilizer

IC : Content of N or P in inflowing water

SSC : Content of N or P in stocked shrimp

SGC : Content of N or P in stocked Gracillaria

SFC : Content of N or P in stocked fish

HSC : Content of N or P in harvested shrimp

HGC : Content of N or P in harvested Gracillaria

HFC : Content of N or P in harvested fish

OC : Content of N or P in outflowing water

Result

Water quality

Table 1 shows that the average concentration of DO in polyculture systems I and

II as well as of inflowing water was in high ranges of more than 4 mg/l. The

average concentration of DO between the polyculture systems during the 90-day

experiment was not significantly different (P>0.05).

Table 1. Mean of water quality parameter over 90 days period (n=3)

Parameter Unit Water input Polyculture I Polyculture II

DO mg/l 4.5 b 5.9 ± 0.7a 5.4 ± 0.6 a

Salinity Ppt 27.7 a 29.3 ± 1.0 a 29.9 ± 0.8 a

Température 0C 27.8 a 26.4 ± 0.05 a 26.9 ± 0.07 a

pH - 7.9 a 8.1 ± 0.1 a 7.9 ± 0.2 a

Alkalinity mg/l 117.6 a 116.4 ± 3.2 a 112.1 ± 2.0 a

H2S mg/l 0 a 0.02 ± 0.001 a 0.03 ± 0.008 a

TSS mg/l 16.3 c 50.5 ± 7.6 a 64.9 ± 4.2 b

Values with the same superscript letter do not differ significantly (P>0.05)

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Table 1 shows that the average salinity for the 90-day experiment was 29.30 ±

1.00 ppt for polyculture I and 29.90 ± 0.80 ppt for polyculture II. Average salinity

was not significantly different between the ponds (P>0.05).

Figure 3 shows a tendency of alkalinity to decrease during the 90-day experiment.

However, the alkalinity was not significantly different between ponds (P>0.05).

Alkalinity in polyculture I ranged between 118.93–109.33 mg/l (Figure 3) with an

average of 116.40 ± 3.20 mg/l (Table 1), while in polyculture II it ranged between

124.80–102.07 mg/l (Figure 3) with an average of 112.10 ± 2.00 mg/l (Table 1).

The average pH over the 90-day experiment was not significantly different

between polyculture I and II (P>0.05), with 8.10 ± 0.10 for polyculture I and 7.90

± 0.20 for polyculture II (Table 1).

Alkalinity

0.00

20.00

40.00

60.00

80.00

100.00

120.00

140.00

0 20 40 60 80 100

Time (days)

Con

cent

ratio

n (m

g/l)

Polyculture I

Polyculture II

water input

b b b

a a aab ab ab

aaaaa

aaaaa a a a a a

Figure 3. Concentration of Alkalinity during the experimental period, values

are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05)

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Total Suspended Solid

0.00

20.00

40.00

60.00

80.00

100.00

120.00

140.00

0 20 40 60 80 100

Time (days)

Conc

entr

atio

n (m

g/l)

Polyculture I

Polyculture II

water input

aa

a a

aa

aa

ba

aa

a c c c c c c c

b bb

b

Figure 4. Concentration of total suspended solid (TSS) during the

experimental period, values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05)

TSS tend to increase and was significantly different between polyculture I and II

(P<0.05). TSS in polyculture I ranged between 10.00–93.67 mg/l, while in

polyculture II it ranged between 11.00–118.33 mg/l (Figure 4). It could be shown

that the differences became obvious at day 60.

Growth performance

Survival rate of shrimp in polyculture II was comparable with polyculture I

(P>0.05). The average survival rate of shrimp in polyculture I during the

production period was 84.4%, while in polyculture II it was 82.8% (Table 2.). The

data showed that mortality rates were low in both systems. Survival rate of fish in

polyculture II at harvest amounted 78.8% (Table 2).

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Table 2. Performance of experimental polyculture system over 90 days period

(n=3)

Parameter Polyculture I Polyculture II

Stocking density:

Shrimp (individual/m2)

Fish (individual/m2)

Total larvae stocked:

Shrimp (ind)

Fish (ind)

Weight of stocked larvae:

Shrimp (g/ind)

Fish (g/ind)

Total weight:

Shrimp (kg)

Fish (kg)

15

-

15000

-

0.43 ± 0.11 a

-

6.45 a

-

15

0.25

15000

250

0.43 ± 0.11 a

4.7 ± 0.6

6.45 a

1.18

Area (m2) 1000 1000

Culture time (days) 90 90

Total Feed (kg) 526.65 a 526.65 a

At harvest:

Shrimp (ind/m2)

Fish (ind/m2)

Weight:

Shrimp (g/ind)

Fish (g/ind)

Total weight:

Shrimp (kg/1000 m2)

Fish (kg/1000 m2)

12.66 a

-

24.73 ± 0.71 a

-

313.08 a

-

12.42 a

0.20

23.45 ± 1.43 a

206.1 ± 11.36

291.25 a

40.67

Survival rate

Shrimp (%)

Fish (%)

84.4 a

82.8 a

78.8

FCR 1.72 a 1.84 a

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SGR:

Shrimp (%/day)

Fish (%/day)

4.5a

4.4 a

4.2 a

Values with the same superscript letter do not differ significantly (P>0.05)

Figure 5 shows that the growth rate of shrimp was not significantly different

between polyculture I and II (P>0.05). The average weight of shrimp at harvest

was 24.73 ± 0.71 and 23.45 ± 1.43 g/ind for polyculture I and II, respectively

(Table 2), while the average fish weight at the time of harvest was 206.1 ± 11.36

g/ind (Table 2). Specific growth rate (SGR) for shrimp in polyculture I and II was

not significantly different (P>0.05) with an average value over the 90-day

experiment of 4.5%/day and 4.4%/day, respectively. SGR of fish over the 90-day

period amounted 4.2% /day.

Weight

0.00

5.00

10.00

15.00

20.00

25.00

30.00

0 20 40 60 80 100

Time (days)

Wei

ght (

g)

Polyculture IPolyculture II

a a aa

a

a

a

a

a aa a

a

aa

a

Figure 5. Individual weight of shrimp during the experimental period, values

are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05)

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Biomass production of shrimp in polyculture I and II was not significantly

different (P>0.05) with an average value of 313.08 and 291.25 kg/1000 m2,

respectively (Table 2). In polyculture II there was an additional production from

the fish of 40.67 kg/1000 m2 (Table 2).

Nutrient flux

The ammonium concentration increased gradually in both polyculture systems

and orthophosphate concentration increased progressively as well. Even though

well water was supplied to the pond at a renewal rate of 2%/day, the ammonium

concentrations in polyculture I increased during the production period from 0.12

to 0.53 mg/l (Figure 6), with an average concentration of 0.34 ± 0.06 mg/l (Table

3). In the polyculture II system, it increased from 0.17 to 0.71 mg/l (Figure 6),

with an average over the production period of 0.45 ± 0.07 mg/l. Therefore,

ammonium concentrations in both polyculture systems did not display significant

differences (P>0.05).

Ammonium

0.0000.100

0.2000.3000.400

0.5000.600

0.7000.800

0 20 40 60 80 100

Time (days)

Conc

entra

tion

(mg/

l)

Polyculture I

Polyculture II

Water input

a

aa a a a

a aa

a ba a a b

bb

a

c c c cc

c c c c

Figure 6. Concentration of ammonium-nitrogen (NH4

--N) during the

experimental period, values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05)

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Orthophosphate

0.0000.0100.0200.0300.0400.0500.0600.0700.080

0 20 40 60 80 100

Time (days)

Con

cent

ratio

n (m

g/l)

Polyculture I

Polyculture II

Water input

c cc c

c c c c c

a aa

a aa

a aa

a aa b b b

b b b

Figure 7. Concentration of orthophosphate (PO4-P) during the experimental

period, values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05)

Orthophosphate in polyculture I increased during the 90-day period from 0.01 to

0.05 mg/l (Figure 7), with an average concentration of orthophosphate of 0.03 ±

0.006 mg/l (Table 3), while in polyculture II it increased from 0.01 to 0.07 mg/l

(Figure 7) with an average of 0.04 ± 0.003 mg/l. These concentrations in both

polyculture systems did not exhibit significant differences (P>0.05).

Nitrite (NO2-) and nitrate (NO3

-) in both polyculture systems did not show

significant differences (P>0.05) with average concentrations of 0.005 ± 0.001

mg/l and 0.05 ± 0.01, mg/l in polyculture I and 0.006 ± 0.001 mg/l and 0.05 ±

0.007 mg/l in polyculture II, respectively (Table 3).

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Table 3. Mean of nutrient concentrations over 90 days period (n=3)

Variable Unit Water input Polyculture I Polyculture II

NH4 mg/l 0.014 b 0.34 ± 0.06a 0.45 ± 0.07 a

NO2 mg/l 0.0002 b 0.005 ± 0.001 a 0.006 ± 0.001 a

NO3 mg/l 0.004 b 0.05 ± 0.01 a 0.05 ± 0.007 a

PO4 mg/l 0.01 b 0.03 ± 0.006 a 0.04 ± 0.003 a

TN mg/l 0.18 b 2.25 ± 0.4 a 2.66 ± 0.8 a

TP mg/l 0.046 b 0.84 ± 0.05 a 0.89 ± 0.05 a

Values with the same superscript letter do not differ significantly (P>0.05)

Additionally, total nitrogen (TN) and total phosphorus (TP) concentration

increased in the outlet water of polyculture systems I and II. TN in the polyculture

I pond increased from 0.40–5.15 mg/l (Figure 8), with an average of 2.25 ± 0.40

mg/l (Table 3) and TN in polyculture II ranged from 0.47–6.16 mg/l (Figure 8),

with an average of 2.66 ± 0.80 mg/l (Table 3). TP in polyculture I increased from

0.03–1.56 mg/l (Figure 9), with an average of 0.84 ± 0.05 mg/l (Table 3), while in

polyculture II values of 0.03–1.64 mg/l (Figure 9) and an average of 0.89 ± 0.05

mg/l (Table 3) could be observed, but no significant differences (P>0.05) could be

calculated between the systems.

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Total Nitrogen (TN)

0.0001.0002.0003.0004.000

5.0006.0007.0008.000

0 20 40 60 80 100

Time (days)

Conc

entra

tion

(mg/

l)

Polyculture I

Polyculture II

Water input

a a aa

a aa

a a

a a aa a a

aa

a

b b b b b b b b b

Figure 8. Concentration of total nitrogen (TN) during the experimental

period, values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05)

Total Phosphorus (TP)

0.0000.2000.4000.6000.8001.0001.2001.4001.6001.800

0 20 40 60 80 100

Time (days)

Con

cent

ratio

n (m

g/l)

Polyculture I

Polyculture II

water inputaa

a

aa a

a

a

aa

aa

aa

aa

b b b b b b b b

Figure 9. Concentration of total phosphorus (TP) during the experimental

period, values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05)

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Mass balance

Total nitrogen (TN) and total phosphorus (TP) from fertilizer amounted 1.56

kg/1000 m2 and 0.2 kg/1000 m2 for polyculture system I and II, respectively.

Whereas TN and TP from inflowing water were 0.5 kg/1000 m2 and 0.13 kg/1000

m2 for both polyculture systems (Figure 10 and 11).

Figure 11. Total nitrogen mass balance in experimental polyculture and

Valueare mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly between

polyculture systems I and II (P>0.05).

TN-mass balance polyculture system I

Outlet water 17.6%

(6.3 kg)a

Water inflow 1.4%

(0.5 kg)a

Figure 10. Total nitrogen mass balance in experimental polyculture systems

I and II. Values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly between polyculture

systems I and II (P>0.05).

Pond WaterFertilization 4.36% (1.56 kg)a

Shrimp feed 94.13%

(33.7 kg)a

Shrimp harvest 46.79% (16.75 kg)a Seaweed harvest

10.56% (3.78 kg)a

rimp stocked06%

(0.02 kg)a

Seaweed stocked0.06%(0.02 kg)a

Others ssociated

25.06%(8.97 kg)a

Sh0. a

Outlet water 17.6%

(6.3 kg)a

Water inflow 1.4%

(0.5 kg)a

Pond WaterFertilization 4.36% (1.56 kg)a

Shrimp feed 94.13%

(33.7 kg)a

Shrimp harvest 46.79% (16.75 kg)a Seaweed harvest

10.56% (3.78 kg)a

rimp stocked06%

(0.02 kg)a

Seaweed stocked0.06%(0.02 kg)a

Others ssociated

25.06%(8.97 kg)a

Sh0. a

 

TN-mass balance polyculture system II

Outlet water 20.6%

(7.4 kg)a

Pond WaterFertilization 4.34% (1.56 kg)a

Shrimp feed 93.79% (33.7 kg)a

Shrimp harvest 41.47% (14.9 kg)a Seaweed harvest

10.94% (3.93 kg)a

Shrimp stocked0.06%(0.02 kg)

Seaweed stocked0.06%(0.02 kg)a

Others associated13.36%(4.8 kg)b

Fish harvest13.64%(4.9 kg)b

Fish stocked0.36%(0.13 kg)

Pond Water

Shrimp0.06%(0.02 kg)a

Fish stocked0.36%(0.13 kg)b

Outlet water 20.6%

(7.4 kg)a

Pond WaterFertilization 4.34% (1.56 kg)a

Shrimp feed 93.79% (33.7 kg)a

Shrimp harvest 41.47% (14.9 kg)a Seaweed harvest

10.94% (3.93 kg)a

Shrimp stocked0.06%(0.02 kg)

Seaweed stocked0.06%(0.02 kg)a

Others associated13.36%(4.8 kg)b

Fish harvest13.64%(4.9 kg)b

Fish stocked0.36%(0.13 kg)

Pond Water

Shrimp0.06%(0.02 kg)a

Fish stocked0.36%(0.13 kg)b

 

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TP-mass balance polyculture system I  

Pond Water

Water inflow 1.95% (0.13 kg)a

Fertilization 3% (0.2 kg)a

Shrimp feed 94.75% (6.32 kg)a

Shrimp harvest 14.99% (1.0 kg)a

Seaweed harvest 9.75% (0.65 kg)a

Outlet water 35.23% (2.35 kg)a

Shrimp stocked0.15%(0.01 kg)a

Seaweed Stocked0.15%(0.01 kg)a

OthersAssociated40.03%(2.67 kg)a

Pond Water

Water inflow 1.95% (0.13 kg)a

Fertilization 3% (0.2 kg)a

Shrimp feed 94.75% (6.32 kg)a

Shrimp harvest 14.99% (1.0 kg)a

Seaweed harvest 9.75% (0.65 kg)a

Outlet water 35.23% (2.35 kg)a

Shrimp stocked0.15%(0.01 kg)a

Seaweed Stocked0.15%(0.01 kg)a

OthersAssociated40.03%(2.67 kg)a

  TP-mass balance polyculture system II

 

Outlet water 37.41%

(2.50 kg)a

Water inflow 1.95%

(0.13 kg)a

Pond WaterFertilization 2.99% (0.2 kg)a

Shrimp feed 94.58%

(6.32 kg)a

Shrimp harvest 13.47% (0.90 kg)a Seaweed harvest

8.83% (0.59 kg)a

Stocked shrimp0.15%(0.01 kg)a

Seaweed stocked0.15%(0.01 kg)a

Others associated35.20%(2.35 kg)b

Fish harvest5.09%(0.34 kg)b

Fish stocked0.18%(0.012 kg)b

Outlet water 37.41%

(2.50 kg)a

Water inflow 1.95%

(0.13 kg)a

Pond WaterFertilization 2.99% (0.2 kg)a

Shrimp feed 94.58%

(6.32 kg)a

Shrimp harvest 13.47% (0.90 kg)a Seaweed harvest

8.83% (0.59 kg)a

Stocked shrimp0.15%(0.01 kg)a

Seaweed stocked0.15%(0.01 kg)a

Others associated35.20%(2.35 kg)b

Fish harvest5.09%(0.34 kg)b

Fish stocked0.18%(0.012 kg)b

 

Figure 11. Total phosphate mass balance in experimental polyculture

systems I and II. Values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly between polyculture

systems I and II (P>0.05).

In polyculture system I shrimp yielded a growth performance of 0.31 kg/m2 and a

feed conversion ratio (FCR) of 1.72, and in polyculture system II equal

performance with 0.29 kg/m2 but additional 0.04 kg fish/m2, at FCR of 1.84.

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Shrimp and seaweed harvested in polyculture system I incorporated in total at

least 57.35% of TN and 24.74% of TP and in polyculture system II higher but no

significantly different (P>0.05) nutrient assimilation of 66.05% for TN and of

27.39% for TP could be found in the total biomass (shrimp, seaweed and fish).

Total nitrogen and phosphorous released with the outlet water amounted 6.3

kg/1000 m2 and 2.35 kg/1000 m2 in polyculture system I. In the polyculture

system II, 7.4 kg/1000 m2 and 2.50 kg/1000 m2 of TN and TP could be found in

the outflowing water, but no significant differences (P>0.05) could be calculated

between the systems.

The largest source of TN originated from feed with 94.13% for the polyculture

system I and 93.79% for the polyculture system II. The remaining nitrogen

derived from fertilizer and inflowing water with 4.36% and 1.4% in polyculture

system I and with 4.34% and 1.39% in polyculture system II (Figure 10). In this

model, the amount of TN from stocked shrimp larvae and seaweed in polyculture

system I was 0.02 kg/1000 m2 and 0.02 kg/1000 m2, respectively. This means

only 0.12% of TN in the ponds derived from stocked biomass in polyculture

system I. In polyculture system II 0.06% and 0.36 % of TN derived from stocked

seaweed and fish (Figure 10).

Outlet water contained 17.6% of TN for the polyculture system I and 20.6% for

the polyculture system II (Figure 10). 25.06% of TN in polyculture system I could

be analyzed as unidentified losses and 13.36% in polyculture system II.

With 94.75% for the polyculture system I and 94.58% for the polyculture system

II largest source of total phosphorus (TP) originated from feed, but without

significant differences (P>0.05) between the systems. The remaining TP derived

from fertilizer and inflowing water with around 3% and 1.95% for both

polyculture systems. TP originated from stocked shrimp larvae and seaweed were

0.15% and 0.15% for both polyculture systems. TP from stocked fish amounted

0.18% in polyculture system II. Total phosphorus (TP) in outlet water was 2.35

kg/1000m² for the polyculture system I and 2.50 kg/1000m² for the polyculture

system II (Figure 11). That means, 35.23% of TP input for the polyculture system

I and 37.41% of TP for the polyculture system II were discharged to the

environment, but no significant differences (P>0.05) could be calculated between

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the systems. 40.03% and 35.20% of TP in polyculture system I and II were

unaccounted and significant differences (P<0.05) could be calculated between the

systems.

Discussion

Results from this study showed, that no significant differences in shrimp

performance between the two polyculture systems could be detected (Table 2).

Shrimp growth and production correlated with stocking density, feeding

management and water quality. The main nutrients were introduced into the ponds

via feed application (Figures 10 and 11). This suggests that pelleted feed may

properly promote nutrient excretion by shrimp and fish that can cause hypoxic

conditions due to decomposition of organic material by bacteria in the bottom

layer of the pond.

As mentioned in materials and method, nutrient fluxes and mass balance were

estimated for various polyculture systems. The water quality in polyculture I and

II (Table 1) was in optimal ranges for fish and shrimp indicated by a high survival

rate (SR) during the 90-day period (Table 2). At the end of the experiment (at

harvest), biomass production of shrimp in polyculture I was higher than

polyculture II (Table 2) but showed clearly not significant differences.

Over the 90 days of the experiment, the feed utilization for increasing shrimp

production was not significantly different in polyculture I and II (P>0.05). It can

be stated that the utilization of feed by shrimp in polyculture I and II was efficient

for growth performance. In comparison to the global average shrimp feed

conversion ratio of around 2.0 (Tacon, 2002), the observed feed conversions in

both polyculture systems were very efficient.

In general, the presence of fish led to lower dissolved oxygen (DO) in polyculture

II than in polyculture I even though it was not significantly different (P>0.05)

(Table 1). In both polyculture systems, aeration was used every night from 22.00

until 05.00. Hydrogen sulphide (H2S) concentration for 90 days was still within

the limits. The average of H2S for polyculture I and II were 0.02 ± 0.001 and 0.03

± 0.008 mg/l (Table 1), respectively. At levels of 0.1–0.2 mg/l H2S in the water,

shrimp growth will be influenced and they will die instantly at concentrations

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higher than 4 mg/l (Law, 1988). Thus, DO concentration and H2S for the 90-day

period were still within the safe limits for shrimp and fish. Additionally DO

concentrations should be linked with seaweed assimilation activities. Its

photosynthesis produces DO that promotes decomposition of organics (Xu, 2008).

The fish in studied polyculture system impacted the amount of suspended solids

by faecal excretion and bioturbation, so that amount of total suspended solids

(TSS) in polyculture II was higher than in polyculture I (P<0.05).

The average concentration of TN and TP in both polyculture systems were not

significantly different (Table 3). Fluctuation of water quality in ponds is normally

a result of variation in nutrients loading from feed and biological processes of

shrimp and organisms in water column (Burford and Williams, 2001). In the

investigation by Briggs and Funge-Smith (1999), ca. 90% of nitrogen input to

their pond came from feed but most of the nitrogen (70-80%) was not retained in

shrimp body, but remained in the pond as accumulated sediment. However,

judging from the higher biomass of shrimp in both polyculture systems (Table 2),

shrimp was considered as a primary organism to process and transform organic

matters from pellet feed to other forms in the water column. Instead of shrimp, our

study obviously indicates that fish and seaweed in ponds play primary roles on

transformation processes of organic matter from pellet feed as well. The high

concentration of nitrogen and phosphorus observed in seaweed was probably

caused from uneaten feed and excretion by the prawns Buschmann (1996). Paez-

Osuna (1999) reported the total nitrogen and phosphorus load from aquaculture to

coastal waters were 54.9% and 57.7%. In this study, TN and TP discharged to the

environment through outlet water in both polyculture systems were lower (Figure

10 and 11). This proves that seaweed and fish are able to utilize nutrients derived

from organic matter of uneaten pellet, and excretory products by the shrimp as

source.

Integrated seaweed aquaculture systems have been suggested as a possible

solution for securing an increasing and environmentally sounded production of

future fish supply (Naylor et al., 2000; Chopin et al., 2001; Troell et al., 2003).

Seaweed has been identified as a marine plant that can reduce the waste of aquatic

animal culture activities in an efficient way (Nelson et al., 2001). A previous

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study showed that seaweed can remove 3.5% of inflowing TN and 2.4% of

inflowing TP (Ihsan et al., submitted). In addition, ammonium in polyculture was

lower than in monoculture systems and amounted 0.24 mg/l while in monoculture

0.37 mg/l could be analyzed. Troell et al. (1997) reported that seaweed have a

high capacity for removing nutrients from fish effluents, and seaweed production

is higher in areas surrounding fish cage than in areas apart from aquaculture

systems. Seaweed had the potential to remove at least 5% of dissolved nitrogen

released from the fish farm and 7% of released dissolved phosphorous.

Buschmann et al. (1994) found that tank cultivated Gracillaria could remove as

much as 90-95% of the ammonium in effluent waters released from salmon tanks.

In this study, nutrient assimilation by seaweed between the two polyculture

systems did not result in significant differences (Figures 10 and 11). Our results

showed a high capacity in assimilation of excretory products from shrimp

nutrients by seaweed in both polyculture systems. The ability of Gracillaria to

assimilate and store nitrogen for ubsequent growth makes it possible to utilize

high nutrient concentrations most efficiently. Such rapid accumulation by

seaweed has been documented to function even in darkness (Cohen and Neori,

1991)

Mass balance model calculated in this study demonstrate nutrient utilization in the

evaluated polyculture systems. TN and TP incorporated in shrimp and seaweed in

polyculture I was lower than polyculture systems II but not significantly different

(Figures 10 and 11). Nutrients were efficiently utilized by shrimp, seaweed and

fish. In comparison to previous results 34.3% of TN and 9.3% of TP were

incorporated in shrimp and Gracillaria of polyculture systems while in

monoculture only 24.2% of TN and 5.3% of TP were retained in shrimp (Ihsan et

al., submitted). Neori et al. (1998) reported that the seaweed harvest contained

about 33% of the total N input and 50% was fed to the animal in the overall N

budget of the abalone tanks and their seaweed biofilter tanks. Lombardi et al.

(2006) reported that shrimp harvesting accounted for 35.5% and 6.1% of the total

nitrogen and total phosphorus input into the ponds in cage polyculture of white

shrimp with seaweed Kappaphycus alvarezii.

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TN and TP incorporated in organism in polyculture system I were higher than in

polyculture system II, while TN and TP discharged to the environment through

outlet water in both polyculture systems did not differ significantly (Figure 10 and

11). Previous results (Ihsan et al., submitted) reported that 44.4% of TN and of

43.3% TP in polyculture systems and 50.4% of TN and 42.8% of TP in

monoculture systems were incorporated in organic biomass, whereas 21.3% and

47.3% of TN and TP were released into the environment in polyculture system in

contrast to 25.4% and 51.9% TN and TP released from monoculture systems,

respectively. Lombardi et al. (2006) reported that outlet water removed significant

quantities of nitrogen (36.7%) and phosphorus (30.3%) in cage polyculture of the

white shrimp and seaweed Kappaphycus alvarezii. Neori and Shpigel (1999)

recorded a reduction in the effluent of 72% of total nitrogen and 61% of total

phosphorus in integrated culture of prawn (Penaeus monodon), mussel (Mytilus

edulis) and seaweed Gracillaria. In polyculture system, TN and other excess

nutrients from the feed based shrimp culture are taken up by seaweed (Martinez-

Aragon et al., 2002). A primary role of biofiltration is the treatment and

conversion of toxic metabolites and pollutants. Microalgae photosynthetically

convert the dissolved inorganic nutrients into particulate matter suspended in the

water, while seaweed in contrast extract the nutrients out of the water (Troell and

Norberg, 1998). Seaweed efficiently take up dissolved inorganic nitrogen present

in fish net pen effluents (Troell et al., 1999). Seaweed growth on polyculture

effluents has been also shown to be superior than in fertilizer enriched seawater

(Neori et al., 1991).

Total nitrogen (TN) and total phosphorus (TP) incorporated in shrimp in this

study did not show significant differences (P>0.05). From the above it can be

stated that the rate of feed utilization by shrimp was optimal, as well as the ability

of seaweed Gracillaria and fish to utilize nutrients in the pond. This proves the

use of polyculture in aquaculture systems in order to improve nutrient utilization

and to decrease nutrient discharge to the environment. However, despite this

relative success, it is necessary to examine other polyculture systems by

integration of other species such as oysters with seaweed, shrimp and fish to

enhance the systems nutrient assimilation performance.

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Conclusion

This study showed that polyculture with shrimp (Penaeus vannamei), fish (Tilapia

sp), and seaweed Gracillaria can be used to increase biomass production.

Inflowing nutrients can be used either by shrimp (Penaeus vannamei), fish

(Tilapia sp) or seaweed Gracillaria (Gracillaria verrucosa). The ability of

seaweed Gracillaria to do photosynthesis caused optimal levels of dissolved

oxygen (DO). The impact of fish as a co-culture organism caused higher total

suspended solids (TSS) in polyculture II than in polyculture I, but it was still

within the safe limits for shrimp.

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Chapter 4: Nitrogen Assimilation Potential of Seaweed

(Gracillaria verrucosa) in Polyculture with Pacific White Shrimps

(Penaeus vannamei)

Y. N. Ihsanab, K. J. Hessec, C. Schulzab

aGesellschaft für Marine Aquakultur mbH, Hafentörn 3, D-25761 Büsum

bInstitute for Animal Breeding and Husbandry, Christian-Albrechts-Universität

D-24098 Kiel

cResearch and Technology Centre, Christian-Albrechts-Universität

D-25761 Büsum

Submitted to the Journal of Asian Fisheries Society

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Abstract

In order to evaluate the nutrient absorption efficiency of combined shrimp and

seaweed production, nitrogen fluxes in polycultures were compared with shrimp

monoculture systems. Therefore, triplicate concrete tanks, with a volume of 3 m3,

were stocked with shrimp Penaeus vannamei (6–7 g, 5 ind/100 litres) and

seaweed (Gracillaria verrucosa) in densities of 0 g/l, 3.125 g/l, 6.250 g/l, and

9.375 g/l. The culture period lasted four weeks and water samples were taken

every week to measure nutrient fluxes. The use of seaweed at a density of 3.125

g/l in shrimp polyculture showed the highest ability for nitrogen assimilation

originating from shrimp waste. This treatment increased shrimp survival rate from

63% (without seaweed) to 83% and the growth performance of shrimp from

247.78 g (without seaweed) to 350.20 g. Remaining nitrogen excreted by shrimp

amounted to 15.36 g, which was mainly (14.62 g) utilized by seaweed to form a

biomass of 16.90 kg. Therefore, polyculture systems using seaweed seem to act

more efficiently with regard to nutrient accumulation.

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Introduction

Shrimp aquaculture has developed quickly since the 1980s in Southeast Asian

countries including Indonesia. However, the rapid industrial growth of

aquaculture has raised environmental concerns about eutrophication and depletion

of natural habitats (Naylor et al., 2000; Zhang, 2003; Zhou et al., 2003; Mao et al.,

2006). Animal mariculture and other anthropogenic activities generate large

quantities of organic and inorganic waste. Especially feed supply results in

excretory products and discharge of uneaten feed, which releases up to 70% of

dietary nutrients into the environment (Porter et al., 1987). Released nutrients

increase eutrophication processes (Neori et al., 1991; Rathakrishnan, 2001) and

the accumulation of acute toxic substances for aquatic animals (Troell et al., 1999;

Neori et al., 2001).

Integrated multitrophic aquaculture techniques are good candidates to overcome

these sustainability problems (Ruddle and Zong, 1988; Primavera, 1991;

Hishamunda and Ridler, 2004). These systems have been proposed as a tool for

developing environmentally sounded aquaculture practices and resource

management within a balanced coastal ecosystem approach (Troell et al., 2003;

Neori et al., 2004). The polyculture of aquatic animals and plants reduces the

environmental impact of the culture system compared to monoculture because of

the reutilization of dissolved and particulate waste products (Petrell et al., 1993).

Seaweed can absorb significant amounts of waste nutrients, controlling

eutrophication, and consequently, improving the health and stability of marine

ecosystems (Buschmann et al., 2001; Chopin et al., 2001; Troell et al., 2003; Fei,

2004; Neori et al., 2004). The physiological mechanisms of seaweed biofiltration

have been studied in, e.g. filter-feeding bivalve culture systems (Fang et al.,

1996), fish cage farms (Troell et al., 1997; Hayashi et al., 2008), shrimp culture

ponds (Jones et al., 2001; Nelson et al., 2001), and polyculture ponds containing

shrimp Penaeus vannamei and seaweed Gracillaria verrucosa (Ihsan et al.,

submitted).

In an aquaculture system most of the nitrogenous and phosphorus dissolved

inorganic waste products are excreted in the form of ammonium (NH4+) and

phosphate (PO43-). Both compounds are potentially toxic to aquatic organisms and

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increase eutrophication potential. The mechanical and chemical treatment and

other processes to remove the excess of ammonium and phosphate from waste

water and the culture ponds are very expensive and may also affect the

environment (Troell et al., 2003). Seaweed has been studied in recent years for

nutrient removal strategies. This treatment technique is considered to be the most

inexpensive and environmentally sounded clearification way (Buschmann et al.,

1996; Rathakrishnan, 2001; Neori et al., 2004).

The subject of the present study is the parameterization of the rate of nitrogen

uptake by the seaweed from shrimp wastewater of polyculture systems in order to

reduce the nutrient releases into the environment.

Material and Method

The experiment was conducted in Sungai Buntu, West Java over a 40-day period

from August–September 2009 in an indoor laboratory facility (Figure 1). This

study used a completely randomized block design conducted in two phases. Phase

I aimed to determine optimal stocking densities and ammonia excretion rates of

shrimps, whereas the second phase quantified the nitrogen assimilation of

seaweed at four seaweed stocking densities.

Figure 1. Map of Research Institute for Brackish water fisheries, West Java,

Indonesia

Location of experiments (Sungai Buntu-West Java)Location of experiments (Sungai Buntu-West Java)

 

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The experiment in phase I was divided into 3 treatments using glass aquaria with

shrimp stocking densities of 5, 10, and 15 ind/100 liters of water. For each

treatment two replications were conducted. Phase I was carried out for 1 week.

The aquarium was filled with 100 liters of aerated sea water, and the environment

was controlled with temperatures in the range of 27–30 °C and salinity ranging

from 25 to 28 ppt. Shrimp were fasted for one day then weighed; afterwards they

were fed for one week and weighed again at the end of the experiment. On the last

day, shrimp were transferred into two containers (10 liters), which had been filled

with aerated sea water and exposed for 8 hours to ultraviolet (UV) light for

disinfection of other nitrogen-consuming organisms. Stocking density in the

containers was one shrimp per 5 liters. Two containers without shrimp served as a

control. Sampling was carried out 6 times at 1 h intervals from 0–5 h. Afterwards

ammonium nitrogen was measured in accordance to APHA standard methods

(1995).

In phase 2, nitrogen assimilation of seaweed at four stocking densities of seaweed

was investigated with 3 replications using concrete tanks (3 m³ volume, 1 m * 3 m

* 1 m). Seaweed stocking densities were 0 g/l (Treatment A), 3.125 g/l (Treatment

B), 6.250 g/l (Treatment C), and 9.375 g/l of seaweed (Treatment D).

Determination of seaweed density was modified from Rathakrishnan (2001).

Shrimp stocking density used in experimental phase 2 amounted 5 shrimp/100

liter with an initial weight of 6–7 g, based on the outcome of growth and survival

results of phase 1 experiments. Individual and total weight of the replicate tank

loading groups was not significantly different (P>0.05).

The shrimp were fed a commercial diet with a protein content of 40% four times a

day, i.e. at 07.00, 12.00, 17.00 and 22.00. The feed quantity was dynamically

assigned to shrimp biomass increase estimated from control sampling. The daily

feed ratio provided 7% of the weight of shrimp at sampling, modified in

accordance with Baliao and Tookwinas (2002). Subsamples of shrimps (number

of individuals) and algae from each tank were weighed every week.

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Sampling

In both phases of the experiment, the following water quality parameters were

measured: temperature, salinity, dissolved oxygen (DO), pH, ammonium, nitrate,

nitrite, and total nitrogen (TN). Additionally, the number and weight of shrimp

and survival rate, growth rate and feed conversion ratio (FCR) were assessed.

In phase 2, every week, ammonium, nitrate, nitrite, and total nitrogen were

analyzed. The samples were taken over a 24-hour period at 3 hour intervals. Water

samples were taken from 20 cm below the water surface. Everyday at 08.00 and

16.00, the water temperature, salinity, and dissolved oxygen (DO) were monitored

in situ with a portable water-quality analyser (TOA model WQC-20A Electronics

Ltd., Japan). Water samples were collected using plastic bottles attached to the

end of a stick. They were immediately filtered through Whatman GF/F filters 0.7

µM millipore for soluble nutrients analyses (NO3-, NO2

-, NH4+). The ammonium

concentration in the filtrate was measured immediately following filtration. Total

nitrogen (TN), nitrate, and nitrite concentrations were measured using the APHA

(1995) standard method. The standard methods for the determination of

ammonium, nitrite and nitrate were based on moderate alkaline solution with

hypochlorite, diazotization, and cadmium reduction followed by diazotization,

respectively. The spectrophotometer wave lengths for ammonium, nitrite, and

nitrate were 630 nm, 542 nm, and 542 nm, respectively. The nutrient analyses

were performed using a spectrophotometer (Shimadzu UV-2400).

The nitrogen content in the feed, shrimp, and seaweed was measured using the

Kjeldahl method. Subsamples of shrimp (quantity) and algae (quantity) were

analyzed at the beginning and the end of the experiment to assess changes in

nitrogenous composition.

Calculation

Survival Rate (SR) was calculated as a ratio of the shrimps quantity at stocking

and sampling time using the following formula:

SR = (Nt / N0) X 100%

With: SR = survival rate

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N0 = number of shrimp on day 0 (individuals)

Nt = number of shrimp on day t (individuals)

Specific growth rate were calculated with the formula (Busacker et al., 1990):

SGR = ((ln Wt - ln W0) / t) * 100%

With: SGR = Specific growth rate

W0 = weight on day-0 (g/individual)

Wt = weight on day-t (g/individual)

t = time of experiment (day)

The feed conversion ratio (FCR) was calculated as the ratio between the amount

of feed given to shrimp biomass increment at a certain period (NRC, 1977) using

the formula:

FCR = F / ΔB

With: FCR = feed conversion ratio

F = amount of feed given during experiment (kg)

ΔB = addition of shrimp biomass during experiment (kg)

Nitrogen retention was calculated based on the following equation:

NR = ∑TNt - ∑TN0

With: NR = Nitrogen retention (g)

∑TNt = amount of total nitrogen on day-t (g)

∑TN0 = amount of total nitrogen on day-0 (g)

Ammonium excretion was calculated based on the following equation (Yigid,

2005):

AE = ((Nt – N0)/(W * Tt-0))

With: AE = Ammonium excretion (mg-N/g/h)

Nt = Ammonium concentration on time-t (mg/l)

N0 = Ammonium concentration on time-0 (mg/l)

W = weight of shrimp (g)

Tt-0= sampling interval

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Statistics

Growth rate, survival rate, nitrogen retention and nutrient fluxes from experiments

were analyzed statistically. All data were checked for normality (Kolmogorov-

Smirnov test) and homogeneity of variances (HOV, Brown Forsythe test).

Differences of means of triplicates in phase 2 were evaluated for significance by

the range tests of Tukey HSD (P<0.05) for homogeneous variance and for

inhomogeneous variances Dunnett-T3 test was used. Calculations were performed

with the SPSS software package (SPSS 9.0.1, 1999).

Result

Phase I

In phase 1, the highest survival rate (SR) and daily weight gain occurred at

densities of 5 ind/100 liters (Table 1). The survival rate (SR) in this density was

100% and average daily growth (ADG) of shrimp was 0.20 g/d. The survival rate

at densities of 10 and 15 ind/100 liters was 80% and 86.7%, respectively. Based

on this data a density of 5 ind/100 liters was proposed for the experimental set up

in phase II.

Table 1. Growth of Shrimp in phase 1

Treatment

(individu)

Unit

Weight

(T0)

Weight

(Tt)

Average

Daily Gain

(g/d)

Survival Rate

(%)

Total average Total Average

5 ind/100 l 34.1 6.8 41.1 8.2 0.20 100.0

10 ind/100 l 75.2 7.5 68.6 8.6 0.15 80.0

15 ind/100 l 107.1 7.1 103.0 7.9 0.11 86.7

During the short-term (5h) ammonium excretion trials, ammonia concentrations in

the containers increased until the 4th hour from 0.45–0.67 mg/l, before starting to

decline during the 5th hour (Table 2). The highest rate of ammonium excretion

was found during the 4th hour (0.67 mg/l). The average (over 5 h) value of

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ammonium excretion was 0.004 mg/g/h. The results of the first phase ammonia

excretion trial are summarized in Table 2.

Table 2. Ammonium Excretion

Containers

Time observation (h)

Weight

of

shrimp

(g)

Ammonium

excretion

(mg/g/h)

0 1 2 3 4 5

Replicate1 0.356 0.438 0.535 0.603 0.671 0.620 7.89 0.005

Replicate2 0.544 0.586 0.540 0.580 0.660 0.643 8.21 0.003

Average 0.450 0.512 0.537 0.591 0.665 0.631 8.05 0.004

Phase II

Growth of shrimp

The total weight of shrimp at the end of the experiment was significantly different

between treatments (P<0.05). The lowest weight of shrimp was 243.78 g in

treatment A (without seaweed), whereas the weight of the other treatment tanks

ranged from 314.71 g to 350.20 g (Table 3). The daily growth rates of shrimp

were not significantly different (P>0.05) among the treatment without seaweed

and the treatment with stocking of seaweed 3.125 g/l (B), 6.250 g/l (C), and 9.375

g/l (D) (Figure 2).

The survival rate (SR) of shrimp in phase II, showed that from the first week until

the end of the study there was a significant difference (P<0.05) in each week

between treatments using seaweed and without seaweed. The SR of shrimp at the

end of experiment in treatment with the seaweed Gracillaria verrucosa (treatment

B, C, and D) were 82.7%, 78.67%, and 76.00%, respectively, while in the

treatment without seaweed (treatment A) was 62.67% (Figure 3). The absolute

survival rate at the end of the experiment was significantly higher in all seaweed

tanks than in the control tanks (without seaweed).

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Table 3. Weight, Retention, and FCR

Treatment

A B C D

Total N-Feed (g) 16.44 18.09 16.9 18.41

Start

Weight shrimp (g) 266.41 265.95 269.74 266.81

N shrimp (%) 7.44 7.43 7.53 7.45

Weight Seaweed (g) 1562.6 3125.26 4688.29

N Seaweed (%) 8.06 16.13 24.19

End

Weight shrimp (g) 243.78a 350.2b 327.96c 314.71d

N shrimp (%) 1.78a 10.16b 9.13b 9.22b

Weight Seaweed (g) 3255.12a 5963.78b 6563.24b

N Seaweed (%) 22.68a 24.67a 36.65b

N-Retention

Shrimp (g) 0.59a 2.73b 1.6c 1.78c

Seaweed (g) 14.62a 8.54b 12.46c

N production of shrimp 15.85a 15.36a 15.3a 16.63a

N in water (g) 15.85a 0.74b 6.76c 4.18c

FCR 2.69a 1.99a 2.02a 2.24a

Daily Growth rate of

Seaweed (%) 2.62a 2.31a 1.20b

Values with the same superscript letter do not differ significantly (P>0.05)

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Weight Average of Shrimp

10.0011.0012.0013.0014.0015.0016.0017.0018.00

0 1 2 3 4 5

Time (Week)

Wei

ght (

g)

Seaweed 0 g/lSeaweed 3.125 g/lSeaweed 6.250 g/lSeaweed 9.375 g/l

a

aa

a

aa

aa

 

Figure 2. Individual weight of shrimp during the experimental period, values

are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05)

Survival Rate

0.00

20.00

40.00

60.00

80.00

100.00

120.00

0 1 2 3 4 5

Time (Week)

Surv

ival

rate

(%)

Seaweed 0 g/l

Seaweed 3.125 g/l

Seaweed 6.250 g/l

Seaweed 9.375 g/l

a a aa

b bb

bbb

 

Figure 3. Survival Rate of shrimp during the experimental period, values are

mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05)

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Growth of seaweed

The daily growth rate of seaweed was significantly different (P<0.05) between

treatments, with the highest average growth rate (2.62 ± 0.06) in the tanks with

lowest seaweed stocking density 3.125 g/l (treatment B) (Table 3). The seaweed

growth rate in the 6.250 g/l seaweed stocking group (treatment C) was

significantly lower (2.31%) than the aforementioned, and the lowest growth rate

(1.20%) was found in the density of 9.375 g/l (treatment D)

Feed conversion ratio (FCR) and nitrogen retention

The FCR of shrimp was not significantly different between treatments (P>0.05).

The lowest FCR value occurred in the treatment with stocking density of seaweed

3.125 g/l (treatment B) i.e. 1.99 and the highest occurred in the treatment without

seaweed (treatment A) i.e. 2.69.

Nitrogen retention of shrimp in each treatment was significantly different

(P<0.05) between treatments. Shrimps that were held in tanks with a low stocking

density of seaweed (3.125 g/l, treatment B) had the highest N-retention (2.73)

whereas in treatment C (stocking seaweed 6.250 g/l) and treatment D (stocking

seaweed 9.375 g/l) were 1.6 and 1.78. The lowest N-retention occurred in

treatment A (without seaweed). Nitrogen retention of seaweed Gracillaria

verrucosa was significantly different (P<0.05) between treatment 3.125 g/l

(treatment B) and the others. Nitrogen retention of seaweed Gracillaria verrucosa

at treatment (B) was 14.62, while in treatment (C) it was 8.54 and (D) 12.46.

Nutrient flux

In this study, the total nitrogen (TN) concentration increased gradually. Figure 4

shows that the concentration of total nitrogen (TN) increased in all treatments. TN

in treatment (A) increased from 0.82 to 2.73 mg/l, while in treatment (B) TN

ranged from 0.65 to 1.67 mg/l and treatment (C) from 0.65 to 1.58 mg/l. The

lowest increase occurred in treatment (D) ranging from 0.55 to 1.46 mg/l. This

means the highest increase of TN occurred in treatment (A), which is significantly

different to other treatments (P<0.05).

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Total Nitrogen

0

0.5

1

1.5

2

2.5

3

3.5

0 1 2 3 4 5

Time (Week)

Conc

entra

tion

(mg/

l)

Seaweed 0 g/l

Seaweed 3.125 g/l

Seaweed 6.250 g/l

Seaweed 9.375 g/la

aa

a

bb

b

bb

b

 

Figure 4. Concentration of total nitrogen (TN) during the experimental

period, values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05)

Ammonium

0

0.2

0.4

0.6

0.8

1

1.2

0 1 2 3 4 5

Time (Week)

Conc

entra

tion

(mg/

l)

Seaweed 0 g/l

Seaweed 3.125 g/l

Seaweed 6.250 g/l

Seaweed 9.375 g/l

a

aa

abb

b

bb

cb

c

d

b

c

 

Figure 5. Concentration of ammonium-nitrogen (NH4--N) during the

experimental period, values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05)

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Even though fresh water was supplied to the ponds, the ammonium-nitrogen

concentrations occurred in different amounts in all treatments. The highest

concentration of ammonium occurred in treatment A (without seaweed) at week 2,

i.e. 0.94 mg/l (Figure 5).

Nitrate showed a different pattern as well. The peak nitrate concentration in all

treatments was 0.009 mg/l. Treatment (A) occurred at week 1, treatment (B) at

week 2, treatment (C) at week 4, and treatment (D) at week 3 (Figure 6). While

nitrite showed the same pattern in all treatments. The peak concentration of nitrite

in all treatments occurred at week 2 and not significantly different (P>0.05).

Treatment (A) was 0.009 mg/l, treatment (B) 0.007 mg/l, treatment (C) 0.008

mg/l, and treatment (D) 0.009 mg/l (Figure 7).

Nitrate

0

0.002

0.004

0.006

0.008

0.01

0.012

0 1 2 3 4 5

Time (WeeK)

Conc

entra

tion

(mg/

l)

Seaweed 0 g/l

Seaweed 3.125 g/l

Seaweed 6.250 g/l

Seaweed 9.375 g/l

a

a

b

a

b

c

a

b

ca

b

c

 

Figure 6. Concentration of Nitrate-nitrogen (NO3--N) during the

experimental period, values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05)

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Nitrite

00.0010.0020.0030.0040.0050.0060.0070.0080.0090.01

0 1 2 3 4 5

Time (Week)

Conc

entra

tion

(mg/

l)

Seaweed 0 g/l

Seaweed 3.125 g/l

Seaweed 6.250 g/l

Seaweed 9.375 g/l

a

a

a

a

a

a

a

a

a

aa

a

 

Figure 7. Concentration of Nitrite-nitrogen (NO2--N) during the experimental

period, values are mean of triplicate ponds (n=3)

Values with the same superscript letter do not differ significantly (P>0.05) 

Discussion

Utilization of dissolved nitrogen by seaweed in the water aims to reduce the waste

burden in the aquaculture media. Nitrogen content of the treatment using the

seaweed was increased but it did not get too high (Figure 4), proving that the

seaweed Gracillaria verrucosa could take up nitrogen. The seaweed could make

use of ammonium through a diffusion process using all parts of its body. The

higher the ability of seaweed to absorb the dissolved ammonium, the greater its

growth. This means that the content of nitrogen will also further increase in the

seaweed biomass, which can be seen from nitrogen seaweed bladder increases.

Nitrogen is necessary for the seaweed in the regulation of metabolism and

reproduction. Growth and biomass can be achieved properly if the seaweed

receives sufficient nitrogen. Uptake of nitrogen by seaweed Gracillaria verrucosa

is not only a function of external nitrogen concentration, but also of the internal

concentration in the plant net. Retrieval and storage of nitrogen by the seaweed

can be affected by the concentration of dissolved inorganic nitrogen in water and

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influenced by ecological fluctuations of nitrogen in plant tissues. Low nitrogen

concentrations in the environment cannot meet the needs of seaweed for nitrogen

for further usage. But the seaweed has the ability to assimilate and store nutrients

from its surroundings, especially at low concentrations. Nitrogen dry weight

content in treatments C and D were lower than treatment B. Presumably, although

the amount of nitrogen in the form of nitrate and nitrite in water is high but

Gracillaria was less able to utilize it. This is consistent with the finding that the

most nitrogen absorbed by the seaweed is nitrogen in ammonium form (Troell et

al., 1999). To meet the need for nitrogen, the reserves stored in the network are

used prior to growth.

The ability of seaweed in taking up nitrogen from shrimp aquaculture waste in

different treatments during the four weeks of maintenance in treatment B,

seaweed was capable of utilizing dissolved nitrogen from shrimp waste up to

14.62 g, so that the weight of seaweed would be increasing twice. If it was

calculated per hour, then the seaweed is capable of absorbing dissolved nitrogen

at a rate of 0.013 g-N/kg/hr. The utilization of nitrogen by seaweed in this study is

higher than the results of the previous study (Ihsan et al., submitted). In the

previous study, the TN of seaweed in polyculture system was 3.5%. In phase 2 of

the study, the absorption of nitrogen by seaweed was three times greater than the

production value of nitrogen excretion of shrimp per hour and kilogram in study

phase I (Table 1). This means that dissolved nitrogen excretion of the shrimp can

be utilized optimally by the seaweed.

Utilization of ammonium at treatments C (6.250 g/l of seaweed) and D (9.375 g/l

of seaweed) is greater than for treatment B (3.125 g/l of seaweed) only at the

beginning of the study (first week). This condition does not last as long as the

amount of ammonium reduced. To meet nutrient needs, seaweed then utilizes

nitrate and nitrite. It can be seen from the steady depletion of nitrate and nitrite

content in aquaculture media. In general, seaweed gradually absorbs nitrogen, i.e.

ammonium> nitrate> nitrite (Troell et al., 1999). Utilization of nitrate and nitrite

by the seaweed is less efficient because nitrate and nitrite must first be reduced

before used by seaweed. Seaweed using nitrate for the metabolism need

involvement of nitrate reductase enzyme (Patadjai, 1993). Absorption of nitrate

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and nitrite by the seaweed is influenced by the concentration of ammonium in the

media. Due to the nitrogen used by seaweed in treatments C and D being nitrate

and nitrite, then the growth of seaweed was not as fast at the beginning of more

research utilizing ammonium. Soriano (2002) reported the growth of seaweed

during the first two weeks as rapid, but that it then declined until the end.

Maintenance of seaweed Gracillaria verrucosa in drain ponds of shrimp in the

first 15 days reached 8.8% and then continued to decline.

Glen et al. (2002) showed that seaweed Gracillaria parvispora cultivation in

shrimp pond effluent water could increase the nitrogen content in the thallus of

1% to 3.5% with a growth rate of 8–9% per day, which is higher than the growth

rate of seaweed fed chemical fertilizers i.e. only 4–5% per day. The content of

ammonium in treatment A (without seaweed) in the second week decreased

drastically. This is due to the oxidation of ammonium into nitrite and then into

nitrate. The content of nitrite and nitrate increased until reaching a peak; this is

due to the aeration of the culture medium so that the oxygen demand for oxidation

processes is met. Boyd (1999) described the process of oxidation with ammonium

as the energy source, CO2 as a carbon source and O2 the source for the oxidation

process. The oxidation process also occurred in treatments B, C, and D but in

small quantities because the ammonium first utilized by seaweed. Besides that,

seaweed also produces oxygen from photosynthesis rest. Xu (2008) reported

Gracillaria cultivation can improve other aspects of water quality instead of

increasing DO. Its photosynthesis produces DO, which promotes decomposition

of organics. Density raft culture of Gracillaria verrucosa impedes the water

circulation and may reduce chemical oxygen demand (COD) in the water column.

In addition, several species of Gracillaria can produce oxygen under low light

conditions, such as in rainy days and remediate anoxia (Xu et al., 2004). Neori et

al. (2004) reported that seaweed Gracillaria sp. is capable of supplying oxygen

(DO) of 2.86 mg/l for 24 hours to the maintenance medium using polyculture with

milkfish, shrimp, and seaweed.

Ammonium concentrations increased again in all treatments during week 4, with

the highest value in treatment (D). This is due to the feeding; the higher residual

and fecal excretion issued shrimp and dead seaweed. Additionally the maximum

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growth of seaweed was achieved in the third week. When maximum growth has

been achieved then the absorption of nitrogen will decrease.

Water quality greatly affects the growth of shrimp. Good water quality is capable

of supporting shrimp life, thereby increasing the appetite of the shrimp. Based on

the value of FCR and the retention of each treatment, it is known that the FCR

indicates the efficiency level of the feed utilization by shrimp as well as affecting

the nutrient waste load discharged into the environment. The smallest FCR

occurred in treatment B (1.99) with a biomass of 350.2 g and survival rate of

82.67%. This means that the high feed utilization by shrimp for growth causes the

retention value also to be high (2.73 g). In comparison to the global average

shrimp feed conversion ratio of around 2.0, the observed feed conversion were

quite good (Tacon, 2002).

The concentration of ammonium and nitrite in treatment (B) was lower compared

with other treatments. To grow the shrimp from 265.95 g to 350.16 g, 15.36 g of

nitrogen waste were generated (Table 3). Most of the waste (14.62 g) was

absorbed by the seaweed, which enabled it to grow to1.69 kg, while the remaining

0.74 g of residual waste remained in the water. The smaller the concentration of

nitrogen remaining in the water, the more effective the utilization rate of nitrogen

by the seaweed.

Conclusions

The seaweed Gracillaria verrucosa can be cultivated in polyculture together with

the shrimp Penaeus vannamei. The ability of seaweed in taking up nitrogen from

the water would make the farming environment better and support shrimp

production. This can be seen from the survival rates (SR) being significantly

different (P<0.05). 

 

 

 

 

 

 

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General Discussion

System performance

In recent years, polyculture system has been proposed as a key to develop

environmentally sounded aquaculture practices and resource management through

a balanced ecosystem approach to avoid pronounced shifts in coastal areas. Feed

based aquaculture needs to be integrated with extractive aquaculture. Multitrophic

polyculture system provides bioremediation potential, mutual benefits to the co-

cultured organism, economic diversification by creating other value added

products and increase profitability per cultivation unit.

In chapter one, based on a literature study polyculture system are described as the

practice of culturing more than one species of aquatic organism in the same

system. The motivating principle is that fish/shrimp production may be

maximized by raising a combination of species having different food habits. The

concept of polyculture of fish/shrimp is based on the concept of total utilization of

different trophic and spatial niches of a pond in order to obtain maximum

fish/shrimp production per unit area (Edward, 1992; Chiang, 1993; Qian et al.,

1996). The main advantages of polyculture systems is that wastes of one resource

user become a source for the others (Neori et al., 2004).

The use of seaweed integrated with fish/shrimp cultures has been studied in open

water and land-based system condition in Israel, Portugal, Brazil, and Indonesia

(Neori et al., 1998; Schuenhoff et al., 2003; Lombardi et al., 2006; Ihsan et al.,

submitted). General concepts about nutrient uptake by seaweed can be found in

Harrison and Hurd (2001). To optimize the seaweed component of an integrated

aquaculture system, particular attention should be given not only to physical and

chemical factors such as light, temperature, effluent nutrient concentration and

flux, and water motion but also to biological factors such as plant variability

including tissue type, plant age, etc.

Xu (2008) reported the Gracillaria cultivation can improve other aspect of water

quality instead of increasing DO. Its photosynthesis produces DO that promotes

decomposition of organics. Density raft culture of Gracillaria impedes the water

circulation and may decrease chemical oxygen demand (COD) in the water

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column. In addition, several species of Gracillaria can produce oxygen under low

light condition, such as in rainy days and remediate anoxia (Xu et al., 2004).

In chapter two, polyculture systems using seaweed Gracillaria seem to act more

efficiently with regard to nutrient accumulation than in monoculture. The average

ammonium-nitrogen concentration over the whole period was 0.24 mg/l in

polyculture while in monoculture 0.37 mg/l of ammonium-nitrogen were

analyzed. Survival rate of shrimp in polyculture and monoculture were 86.32%

and 69.17%, respectively.

Growth performance

Overall, the growth performance of shrimp in polyculture was better than

monoculture systems. In chapter two, the average final weight of shrimp was 24.9

± 1.8 g for polyculture systems with survival rates of 86.3%. For monoculture, the

weight of shrimp was 20.8 ± 1.05 g and survival rate accounted 69.17%. Survival

rate of shrimp in polyculture was significantly higher than in monoculture, and the

weight of shrimp as well. The feed conversion ratio (FCR) for the polyculture and

monoculture system in this study were significantly (P<0.05) different with 1.67

and 1.88, respectively. In comparison to global average shrimp feed conversion

ratio of around 2.0, observed feed conversions were quite good (Tacon, 2002).

In chapter three, the growth rate of shrimp was not significantly different between

polyculture I and II (P>0.05). The average weight of shrimp at harvest was 24.73

± 0.71 and 23.45 ± 1.43 g/ind for polyculture I and II, respectively. Specific

growth rate (SGR) for shrimp in polyculture I and II was not significantly

different (P>0.05) with an average value over the 90-day experiment of 4.5%/day

and 4.4%/day, respectively.

Shrimp growth and production were reported to be basically related to the

environmental condition (Songsangjinda, 1994). Results from this study showed

clear differences in performance parameters between monoculture and polyculture

systems. This result may indicate that seaweed play a vital role on system

productivity. This result is in agreement with the observation of Troell et al.

(1997) and Soriano et al. (2002). They reported that the environmental conditions

for growth of shrimp in polyculture systems is better than in monoculture. Apart

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from removing nutrients, the seaweed as co-cultured organisms may contribute to

the oxygen budget of the ponds.

Fluctuation of water quality in ponds is the result of variation in nutrients loading

from feed and biological processes of shrimp and organisms in water column

(Burford and Williams, 2001).

In chapter three, the water quality in polyculture systems were in optimal ranges

for fish and shrimp indicated by a high survival rate (SR) during the 90-day

period. Results from this study showed, that no significant differences in shrimp

performance between the two polyculture systems. Shrimp growth and production

correlated with stocking density, feeding management and water quality. The

main nutrients were introduced into the ponds via feed application. This suggests

that pellet feed may properly promote nutrient excretion by shrimp and fish that

can cause hypoxic conditions due to decomposition of organic material by

bacteria in the bottom layer of the pond.

Nutrient flux

The two significant components of the pond environment are the pond water and

sediment which interact continuously to influence the culture environment. Pond

sediment can be further divided into the pond soil component (the pond bottom

and walls) and the accumulated sediment component (Briggs and Funge-Smith,

1994). In the investigation by Funge-Smith and Briggs (1998), around 90% of

nitrogen input to the pond came from feed but most of the nitrogen (70-80%) was

not retained in shrimp body, but remain in the pond as accumulated sediment.

In chapter two, the ammonium concentration increased gradually in monoculture

and polyculture systems and orthophosphate concentration progressively

increased as well. Though well water was supplied to the pond, the ammonium-

nitrogen concentrations in monoculture increased from 0.005 to 0.779 mg/l, with

an average concentration of ammonium-nitrogen during the 100 days period of

0.37 mg/l. In polyculture system, it increased from 0.003 to 0.483 mg/l, with an

average of 0.24 mg/l. Therefore, ammonium-nitrogen concentrations in

monoculture system were significantly higher in comparison to polyculture

system (P<0.05), in which Gracillaria assimilated ammonium from water.

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Ideally, nutrient process in polyculture system with two or more ecologically

compatible species should be balanced, waste from one species are recycled as

fertilizer or feed by another without conflicting with each other (Neori et al.,

2000). By integrating fed mariculture (fish and shrimp) with extractive

mariculture (seaweed), the wastes of one resource consumer become a source

(fertilizer or feed) for others in the system. To get more information about

optimum nutrient utilization, the absorbtion of nitrogen derived by shrimp waste

into seaweed Gracillaria verrucosa is described in chapter four.

In chapter four, the total nitrogen (TN) concentration increased gradually. It

shows that the concentration of total nitrogen (TN) increased in polyculture and

monoculture system. The highest increase of TN occurred in monoculture system

(treatment without seaweed) from 0.82 to 2.73 mg/. The lowest increase occurred

in polyculture using seaweed at stocking densities of 9.375 g/l (treatment D)

ranging from 0.55 to 1.46 mg/l.

Mass balance

In chapter two, a mass balance model was developed for total nitrogen and total

phosphorus to estimate their fluxes. From the total nitrogen and total phosphorus

input, 24.2% and 5.3% were incorporated in 335.7 kg/1200 m2 shrimp weight gain

in monoculture, while 30.8% and 6.9% were incorporated in 501.5 kg/1200m2

shrimp weight gain and 3.5% and 2.4% were incorporated in 325 kg/1200 m2

seaweed Gracillaria in polyculture system.

In chapter three, mass balance model in this study showed nutrient utilization in

the evaluated polyculture systems. TN and TP incorporated in shrimp and

seaweed in polyculture I was lower than polyculture systems II but not significant

different.

Conclusion

Responsible aquaculture practices should be based on a balanced ecosystem

management approach, which incorporate the biological and environmental

function of a diverse group of organisms into a unified system that maintains the

natural interaction of species and allows an ecosystem to function sustainable. In

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general, shrimp and fish aquaculture using additional feed produces a large

amount of waste, including nitrogen and phosphorus that could be released into

the aquatic environment if not treated.

Integrated seaweed aquaculture systems have been suggested as a possible

solution for securing an increasing and environmentally sounded production of

future supply.

Normally, production of main target organism in polyculture system could

decrease due to competition in space and nutrient utilization with co-cultured

organisms. The results in this study suggest that seaweed can not only serve as an

effective biofilter for shrimp ponds but also can increase shrimp production even

integrated with fish within the same system. The weight and survival rate of

shrimp in polyculture systems were higher than in monoculture.

The ability of seaweed in taking up nitrogen from the water would make the

farming environment better and support shrimp production. Thus polyculture

systems using seaweed seem to act more efficiently with regard to nutrient

accumulation.

References

Briggs, M. R. P., and Funge-Smith, S. J. 1994. A nutrient budget of some

intensive marine shrimp ponds in Thailand. Aquacult. Fisheries Manage.

25:789-811.

Chiang, Y. M. 1993. Seaweed cultivation in Taiwan. In Liao, I. C., Cheng, J. H.,

Wu, M. C., Guo, J. J. (Eds.) Proc. Symp. On Aquaculture held in Beijing,

21-23 December 1992. Taiwan Fisheries Research Institute, Keelung, pp.

143-51

Edward, P. 1992. Reuse of human wastes in aquaculture, a technical review.

Water and sanitation report no 2. UNDP-World Bank Sanitation Program.

World Bank. Washington, DC. Pp, 33-50.

Funge-Smith, S. J. and M. R. P. Briggs. 1998. Nutrient budgets in intensive

shrimp ponds: implications for sustainability. Aquaculture. 164. 117-133.

Harrison, P. J., and Hurd, C. L. 2001. Nutrient physiology of seaweeds:

application of concepts to aquaculture. Cah. Biol. Mar. 42:71-82

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Ihsan, Y. N, K. J. Hesse, N Holmgren, C Schulz. Submitted. A Comparison of

Nutrients Fluxes in Monoculture and Polyculture Systems for Shrimp

(Penaeus vannamei) and Seaweed (Gracillaria verrucosa) Production.

Submitted to the journal of World Aquaculture Society.

Lombardi, J. V., de Almeida-Marques, H. L., Pereira, R. T. L., Barreto, O. J. S.,

de Paula, E. J. 2006. Cage polyculture of the Pacific white shrimp

Litopenaeus vannamei and the Philippines seaweed Kappaphycus

alvarezii. J. Aquacult. 258:412-415.

Neori, A., Ragg, N. L.C., Shpigel, M. 1998. The integrated culture of seaweed,

abalone, fish and clams in modular intensive land-based systems: II.

Performance and nitrogen partitioning within an abalone (Haliotis

tuberculata) and macroalgae culture system. Aquacult. Eng. 17:215-239.

Neori, A., T. Chopin T, M. Troell, A. H. Buschmann, G.P. Kraemer, C. Halling,

M. Shpigel, C Yarish. 2004. Integrated aquaculture: rationale, evolution

and state of the art emphasizing seaweed biofiltration in modern

mariculture. Aquaculture 231:361–391.

Qian, P. Y., C. Y. Wu, M. Wu, Y. K. Xie. 1996. Integrated cultivation of red alga

Kappaphycus alvarezii and the pearl oyster Pinctada martensi.

Aquaculture 147: 21-35

Schuenhoff, A., Shpigel, M., Lupatsch, I., Ashkenazi, A., Msuya, F. E., Neori, A.

2003. A semi-recirculating, integrated system for the culture of fish and

seaweed. Aquaculture 221:167–181.

Soriano, E. M., C Morales, W. S. C Moreira. 2002. Cultivation of Gracillaria

(Rhodophyta) in shrimp pond effluents in Brazil. Aquaculture Research

33: 1081-1086.

Tacon, A. G. J. 2002. Thematic review of feed and feed management practices in

shrimp aquaculture. Report prepared under the World Bank, NACA,

WWF and FAO consortium program on shrimp farming and the

environment, published by consortium. 69.

Troell, M., C Halling, A Nilsson, A. H Buschmann., N Kautsky, L Kautsky. 1997.

Integrated marine cultivation of Gracilaria chilensis (Gracilariales,

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Bangiophyceae) and salmon cages for reduced environmental impact and

increased economic output. Aquaculture 156:45–61.

Xu, Y. J., N. Z. Jiao, L. M. Qian. 2004. Nitrogen nutritional identities of

Gracillaria as bioindicators and restoral plants (in Chinese with English

abstract). Journal of Fishery Sciences of China. 11. 276-281.

Xu, Y. J., J. Fang, Q. Tang, J. Lin, G. Le. 2008. Improvement of water quality by

the macroalga, Gracillaria lemaneiformis (Rhodophyta), near aquaculture

effluent outlets. World aquaculture society. 39. 549-555. 

 

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General Summary

Feed based shrimp and fish aquaculture produces a large amount of waste,

including nitrogen and phosphorus that is released to the aquatic environment

without treatment. The present thesis is focussed on various polyculture systems

using shrimp Penaeus vannamei, fish Oreochromis sp. and seaweed Gracillaria

verrucosa. Seaweed cultivation in integrated polyculture system appears to be a

viable approach to reduce nutrients discharge to the environment. Seaweed can be

efficient in removing nutrients from effluents of intensive fish and shrimp farm.

By integrating fed with extractive forms of aquaculture, the wastes of one

resource user become a source for the others.

Chapter one presents an introduction of nutrient fluxes in various polyculture

systems and implication for its sustainability. A review of scientific literature

illustrates important aspects to implement polyculture system using seaweed as

biofilter. The production of seaweed in cage culture can be successfully integrated

in the production of fish and shrimp. Regarding the environmental benefits of

integrated seaweed and fish or shrimp production, seaweed culture can also

benefit by increasing their economic viability. Integrated seaweed aquaculture

systems have been suggested as a possible solution for securing an increasing and

environmentally sounded production of future supply of fish and seafood.

Chapter two compares performance and nutrient fluxes of monoculture and

polyculture system. Therefore triplicate ponds of 1200 m² were stocked with

seaweed (0.04 kg/m²) and 20 individuals of shrimp (0.22 ± 0.016 g/ind)/m2. The

culture period lasted 100 days and water samples to describe nutrient fluxes were

taken every 10 days. Results indicate that polyculture systems using seaweed

seem to act more efficiently with regard to nutrient accumulation. The average

ammonium-nitrogen concentration over the whole period was 0.24 mg/l in

polyculture while in monoculture 0.37 mg/l of ammonium-nitrogen were

analyzed. From the total nitrogen and total phosphorus input, 24.2% and 5.3%

were incorporated in 335.7 kg/1200 m2 shrimp weight gain in monoculture, while

30.8% and 6.9% were incorporated in 501.5 kg/1200m2 shrimp weight gain and

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3.5% and 2.4% were incorporated in 325 kg/1200 m2 seaweed in polyculture

system.

A comparative study on polyculture systems using various combinations of

shrimp, seaweed and fish was conducted in chapter three in order to calculate

nutrients fluxes and mass balances. Therefore, triplicate ponds of 1000 m2 size

were stocked with 0.4 kg/m2 seaweed and 15 shrimps/m2 (polyculture I), and

triplicate ponds of size 1000 m2 were stocked with 0.4 kg/m2 seaweed, 15

shrimps/m2, and 0.25 fish/m2 (polyculture II). A mass balance model was

developed for total nitrogen and total phosphorus to estimate their fluxes. From

total nitrogen and total phosphorus input, 46.79% and 14.99% were incorporated

in 313.08 kg/1000 m2 shrimp weight gain in polyculture system I, while 41.47%

and 13.47% were incorporated in 291.25 kg/1000 m2 shrimp weight gain and

13.64% and 5.09% were incorporated in 40.67 kg/1000 m2 fish weight gain in

polyculture system II. These results suggest that no significant differences in

shrimp performance between the two polyculture systems (P>0.05) could be

observed.

Chapter four evaluated the nutrient absorption efficiency of combined shrimp and

seaweed production. Therefore, triplicate concrete tanks, with a volume of 3 m3,

were stocked with shrimp (6–7 g, 5 ind/100 litres) and seaweed in densities of 0

g/l, 3.125 g/l, 6.250 g/l, and 9.375 g/l. The use of seaweed at a density of 3.125 g/l

in shrimp polyculture showed the highest ability for nitrogen assimilation

originating from shrimp waste. This treatment increased shrimp survival rate from

63% (without seaweed) to 83% and the growth performance of shrimp from

247.78 g (without seaweed) to 350.20 g. Remaining nitrogen excreted by shrimp

amounted to 15.36 g, which was mainly (14.62 g) utilized by seaweed to form a

biomass of 16.90 kg. Therefore, polyculture systems using seaweed seem to act

more efficiently with regard to nutrient accumulation and beneficial effects on co-

cultured organisms.

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Zusammenfassung

Die futtermittelbasierte Aquakultur kann zu einer Anreicherung von

Stoffwechselendprodukten führen, die die Qualität des genutzten Gewässers

erheblich beeinträchtigen können. In der vorliegenden Arbeit wurde deshalb die

Reduzierung von Nährstoffemissionen der Aquakultur durch multitrophe

Haltungssysteme untersucht. Hierzu wurden verschiedene Kulturverfahren von

Tilapia, Shrimp und Makroalgen unter praxisgleichen Bedingungen in Indonesien

untersucht.

Kapitel eins der vorliegenden Arbeit führt thematisch ein und beschreibt die

grundlegenden Prozesse im Nährstoffkreislauf von Gewässer- und

Aquakultursystemen. Aufgrund der vielfältigen gelösten und partikulären

Nährstofffraktionen in Aquakultursystemen kann nur auf Basis von multitrophen

Systemen eine relevante Nährstoffausnutzung realisiert werden. Anhand vieler

Untersuchungen aus der Literatur kann dabei auf die besondere Bedeutung von

Algen als Biofilter in einem Polykultur-System hingewiesen werden, da deren

hohe Wachstumspotentiale die anfallenden gelösten Stickstoff- und

Phosphorverbindungen der tierischen Aquakulturproduktion effektiv verwerten,

die Haltungsumwelt für weitere Organismen optimieren und der zusätzlichen

ökonomischen Wertschöpfung dienen. Weiterhin bietet sich die kombinierte

Aufzucht von carnivoren mit omni- oder herbivioren Species an, da somit die

Stoffwechselendprodukte in der niedrigeren Trophieebene effektiv in Biomasse

überführt werden können.

In Kapitel zwei werden die Potentiale von Monokultur- und Polykultursysteme

experimentell miteinander verglichen. Dafür wurden drei Teiche mit identischer

Fläche von 1200 m2 in Polykultur mit Gracillaria verrucosa (50 kg) und 20

Shrimps/m² (Penaeus vannamei, Anfangsgewicht 0.22 ± 0.016 g) besetzt.

Weiterhin dienten 3 Teiche mit Shrimpmonokultur bei Besatzdichten von 20

Shrimps/m² als Vergleich. Der Versuch wurde über 100 Tage durchgeführt und im

Abstand von 10 Tagen wurden die Wasserinhaltsstoffe erfasst. Die Werte

indizieren, dass das Polykultur-System mit Algen Gracillaria effizienter die

zugeführten Nährstoffe in Biomasse überführen. Die Durchschnittskonzentration

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von Ammonium-Stickstoff über die gesamte Versuchsperiode betrug

beispielsweise 0.24 mg/l im Polykultur- und 0.37 mg/l im Monokultursystem. In

der Nährstoffbilanzierung zeigt sich, dass aus dem gesamten Stickstoff (TN)- und

Phosporeintrag (TP) 24.2% bzw. 5.3% in 335.7 kg Shrimpsbiomasse in der

Monokultur überführt wurde, während in der Polykultur 30.8% bzw. 6.9% des

eingetragenen TN und TP in 501.5 kg Shrimps und 3.5 % bzw. 2.4% des TN und

TP in 325 kg Makroalgen Gracillaria verrucosa eingebaut wurden.

Im dritten Kapitel wurden das Polykulturverfahren mit Gracillaria-Algen und

Shrimp (Peneaus vannamei, Polykultur I) mit einem dreigliedrigen Verfahren aus

Shrimp (Peneaus vannamei), Fisch (Oreochromis niloticus) und Makroalgen

(Gracillaria verrucosa, Polykultur II) verglichen. Hierfür wurde wiederum ein

triplikater Versuchsansatz mit jeweils drei Teichen mit einer Fläche von 1000 m2

eingesetzt und mit 0.4 kg/m2 Makroalgen und 15 Shrimps/m2 besetzt. In die

dreigliedrigen Polykultursystemteiche wurden zusätzlich 0.25 Fische/m² gesetzt.

Das Fütterungsmanagement berücksichtigte lediglich die Shrimps, die in beiden

Versuchsansätzen mit vergleichbarer Intensität gefüttert wurden. In der

Nährstoffbilanz zeigte sich, dass in Polykultur I aus dem TN- und TP-Eintrag

46.70% und 14.99% in 313.08 kg Shrimpbiomasse umgesetzt wurde, während in

Polykultur II 41.7% und 13.47% in 291.25 kg Shrimps und 13.62% und 5.09% in

40.67 kg m2 Fisch eingebaut wurden. Die Makroalgen inkorporierten in

Polykultur I 10.56 % und 9.75 % TN und TP, und in Polykultur II vergleichbare

10.94% und 8.83%. Dieses Ergebnis zeigt, dass das Shrimpsaufkommen durch die

Polykultur mit Fischen nicht signifikant beeinträchtigt wird, durch die zusätzliche

Nährstoffbindung jedoch signifikant weniger Nährstoffe aus dem System geführt

werden.

Im abschließenden vierten Kapitel wurde das Nährstoffaufnahmepotential von

variierendem Makroalgenbesatz in Polykultur mit Shrimps untersucht. Dafür

wurden in kleinskaligen Betonsystemen mit einem Volumen von 3 m3 Garnelen,

Penaeus vannamei, (6-7 g, 5 Ind/100 Liter) und Makroalgen Gracillaria

verrucosa bei verschiedenen Kulturdichten von 0 g/l, 3.125 g/l, 6.250 g/l und

9.375 g/l aufgezogen und die Wachstumsleistungen und Nährstoffbilanzen

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ermittelt. Dabei zeigte sich, dass die Stickstoffaufnahme der Makroalgen bei einer

Besatzdichte von 3.

125 g/l am höchsten ist. Zudem kann eine positive Wirkung auf die Shrimps

festgestellt werden, da sich höhere Wachstumsleistungen (Gesamtendgewicht:

243.78 g ohne Algen; 350.20 g bei Algendichte: 3.125 g/l) und

Überlebensleistungen der Shrimps (63% ohne Algen, 83% bei Algendichte von

3.125 g/l) einstellen. Der aus der Shrimpfütterung stammende Stickstoff (15.36 g)

wurde dabei überwiegend (14.62 g) von den Algen zur Biomassebildung genutzt.

Schlussfolgend kann gesagt werden, dass die gezielte Polykultur von Shrimps-,

Fisch und Makroalgenaufzucht zu einer deutlich verbesserten

Nährstoffausnutzung und damit zu geringeren Nährstoffausträgen aus

Aquakulturen führen können. Die Zusammenhänge zwischen den

unterschiedlichen trophischen Produktionsebenen sind jedoch nur in Teilen

verstanden, so dass weiterhin ein sehr großes Optimierungspotential besteht.  

 

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Danksagung

An dieser Stelle möchte ich den Menschen Dank entgegenbringen, die zum

Gelingen der vorliegenden Arbeit beigetragen haben.

Ich bedanke mich bei meinem Betreuer Herrn Prof. Dr. Carsten Schulz für die

Überlassung des interessanten Themas und das mir geschenkte Vertrauen bei der

Projektbearbeitung.

Herrn Dr. Karl J. Hesse vom FTZ-Buesum und Prof. Dr. Nöel Holmgren der

Universität zu Skövde-Sweden danke ich für die Diskussion.

Dank gilt meinen lieben Kolleginnen und Kollegen vom FTZ/Corelab für die

Unterstützung bei der Versuchsdurchführung und die überaus schöne Zeit in Kiel

und Büsum. Besonders bei Herrn Prof. Dr. Roberto Mayerle, Dr. Peter Weppen,

Britta Egge und Daniela Koch bedanke ich mich, dass ich als Gast in FTZ/Corelab

arbeiten durfte.

Den Kollegen aus Indonesien danke ich für die gute Zusammenarbeit.

Ich bedanke mich bei Herrn Dede Suhendar für die Hilfsbereitschaft bei der

Versuchsdurchführung und die angenehme Büronachbarschaft.

Meinen Eltern danke ich für die wie immer selbstlose Unterstützung jeglicher Art.

Und ganz besonders danke ich euch, Aminuddin Shaleh und Mulyati Aminuddin,

weil ihr mir allzeit Kraft gebt

Mein größter Dank an meine Frau Tri Dewi K P und meine Kinder, Azka Auliya

Yudanegara, Gilang Auliya Fauzin und Fadhlan Auliya Danurdoro für ihre

Unterstützung.

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  108

Lebenslauf

Name: Yudi Nurul Ihsan

Geburstag: 1.12.1975

Gebursort: Bandung – Indonesien

Eltern: Aminuddin Shaleh

Mulyati Aminuddin

Schulausbildung:

1982-1988 SD Melong Asih II Bandung - Indonesien

1988-1994 SMAM Garut - Indonesien

Studium:

1994-1999 Bachelor-Studium “Aquaculture“ an der Bogor Agricultural

University zu Bogor (IPB-Bogor) Indonesien

1999-2002 Master-Studium “Coastal and Marine Resource

Management“ an der Bogor Agricultural University zu

Bogor (IPB-Bogor) Indonesien

Berufliche Tätigkeit:

2002-2005 Wissenschaftliche Mitarbeiter am Center for Coastal and

Marine Resources Study (CCMRS-IPB) Bogor, Indonesien

2005-2008 Wissenschaftliche Mitarbeiter an der Fisheries and Marine

Sciences Fakultät, Universitas Padjadjaran Bandung,

Indonesien

2008-2011 Wissenschaftliche Mitarbeiter bei der Gesellschaft für

Marine Aquakultur (GMA) mbH in Büsum bei Herrn Prof.

Dr. C. Schulz