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Aus dem <strong>Institut</strong> <strong>für</strong> Tierzucht und Tierhaltung<br />
der Agrar- und Ernährungwissenschaftlichen Fakultät<br />
der Christian-Albrechts-Universität zu Kiel<br />
NUTRIENT FLUXES IN MULTITROPHIC<br />
AQUACULTURE SYSTEMS<br />
Dissertation<br />
zur Erlangung des Doktorgrades<br />
der Agrar- und Ernährungwissenschaftlichen Fakultät<br />
der Christian-Albrechts-Universität zu Kiel<br />
vorgelegt von<br />
Master of Science<br />
YUDI NURUL IHSAN<br />
aus Bandung - Indonesien<br />
Kiel, 2012<br />
Dekan<strong>in</strong>: Prof. Dr. K. Schwarz<br />
Erster Berichterstatter: Prof. Dr. C. Schulz<br />
Zweiter Berichterstatter: Prof. Dr. E. Hartung<br />
Tag der mündlichen Prüfung: 09.02.2012
Gedruckt mit Genehmigung der Agrar- und Ernährungswissenschaftlichen<br />
Fakultät der Christian-Albrechts-Universität zu Kiel<br />
II
Table of Contents<br />
General Introduction ....................................................................................................... 1<br />
Chapter 1:<br />
Nutrient flux <strong>in</strong> polyculture system us<strong>in</strong>g seaweed as biofilter: Implication for<br />
susta<strong>in</strong>ability............................................................................................................... 5<br />
Chapter 2:<br />
A Comparison of <strong>nutrient</strong> <strong>fluxes</strong> <strong>in</strong> monoculture and polyculture <strong>systems</strong> for<br />
shrimp (Penaeus vannamei) and seaweed (Gracillaria verrucosa) production...... . 20<br />
Chapter 3:<br />
Nutrient Fluxes and Mass Balances <strong>in</strong> Various Polyculture Systems Us<strong>in</strong>g<br />
Shrimp Penaeus vannamei, Fish Oreochromis sp. and Seaweed Gracillaria<br />
verrucosa................................................................................................................. 46<br />
Chapter 4:<br />
Nitrogen Assimilation Potential of Seaweed Gracillaria verrucosa <strong>in</strong><br />
Polyculture with Pacific White Shrimps (Penaeus vannamei) .............................. 74<br />
General Discussion ...................................................................................................... 95<br />
General Summary......................................................................................................... 102<br />
Zusammenfassung........................................................................................................ 104<br />
Danksagung.................................................................................................................. 107<br />
Lebenslauf.................................................................................................................... 108<br />
III
General Introduction<br />
The mar<strong>in</strong>e sector <strong>in</strong>clud<strong>in</strong>g <strong>aquaculture</strong> is one of the lead<strong>in</strong>g sectors <strong>in</strong> economic<br />
development <strong>in</strong> the world. Aquaculture contributes significantly to food<br />
availability, household food security, <strong>in</strong>come generation, trade, and improved<br />
liv<strong>in</strong>g standards <strong>in</strong> Indonesia. In poor rural communities, <strong>aquaculture</strong> can be an<br />
<strong>in</strong>tegral component of development contribut<strong>in</strong>g to susta<strong>in</strong>able livelihoods and<br />
enhanc<strong>in</strong>g social well-be<strong>in</strong>g. S<strong>in</strong>ce 1990 the gap between the demand for and<br />
supply of fish has been widen<strong>in</strong>g rapidly due to the decl<strong>in</strong>e of capture fisheries<br />
production and a cont<strong>in</strong>ually grow<strong>in</strong>g population. Aquaculture is forecasted to<br />
dom<strong>in</strong>ate, if not surpass, the importance of mar<strong>in</strong>e capture fisheries <strong>in</strong> provid<strong>in</strong>g<br />
high quality animal prote<strong>in</strong> to lower <strong>in</strong>come groups, employment, and export<br />
earn<strong>in</strong>gs.<br />
Indonesia has good fisheries and <strong>aquaculture</strong> potential. Because of its rich, coastal<br />
and mar<strong>in</strong>e resources suitable for <strong>aquaculture</strong> development, it is one country<br />
where <strong>aquaculture</strong> can contribute to economic and social development goals. The<br />
potential area for <strong>aquaculture</strong> is estimated at about 26 million hectares (ha),<br />
consist<strong>in</strong>g of 24.5 million ha of coastal areas suitable for mariculture, 913<br />
thousand ha of brackish water areas, and 1.1 million ha of freshwater areas.<br />
Actual area coverage of <strong>aquaculture</strong> is currently estimated at only 681 thousand<br />
ha, correspond<strong>in</strong>g to less than 3% of the total potential area.<br />
The contribution of fish to global human food supply has reached a record of<br />
about 17 kg per person <strong>in</strong> average, supply<strong>in</strong>g over three billion people with at<br />
least 15% of their average animal prote<strong>in</strong> <strong>in</strong>take (FAO, 2010). Mar<strong>in</strong>e <strong>aquaculture</strong><br />
has been a rapidly grow<strong>in</strong>g <strong>in</strong>dustry, <strong>in</strong>creas<strong>in</strong>g from about 18.6 million tons <strong>in</strong><br />
2006 to 20.1 million tons <strong>in</strong> 2009 and these patterns are expected to cont<strong>in</strong>ue up to<br />
2030 due to the <strong>in</strong>creas<strong>in</strong>g global demand and high market value of <strong>aquaculture</strong><br />
products (FAO, 2010). Global production of shrimp has <strong>in</strong>creased by more than<br />
600% between 1989 and 2009 and is expected to cont<strong>in</strong>ue due to the high market<br />
value of cultured shrimp. This production comes from a variety of farms rang<strong>in</strong>g<br />
from small-scale ponds to large-scale ponds.<br />
As a result of the rapid production <strong>in</strong>crease, it is not unreasonable to conceive that<br />
<strong>aquaculture</strong> activities might affect the environment <strong>in</strong> a variety of ways, especially<br />
1
fish and shrimp <strong>aquaculture</strong> which need to supplemented with an exogenous<br />
source of <strong>nutrient</strong>s. Increased production is be<strong>in</strong>g achieved by expansion of land<br />
and water areas under culture and <strong>in</strong>volve higher utilization of production <strong>in</strong>puts<br />
such as water, feeds, fertilizers, and chemicals. Higher <strong>in</strong>puts normally affect the<br />
surround<strong>in</strong>g environment <strong>in</strong> a number of ways. Particular concern arise by the<br />
effects of particulate nitrogeneous wastes produced by the ponds <strong>in</strong> the form of<br />
uneaten feed and fish faeces (Pearson and Gowen, 1990; Troell et al., 2003).<br />
Poorly managed coastal shrimp farms have been cited for degrad<strong>in</strong>g nearshore<br />
habitats through <strong>nutrient</strong> enrichment (Boyd, 1999; Hargreaves, 1998). Nutrient<br />
enrichment could also affect the shrimp farms themselves through self-pollution.<br />
Poor water quality may reduce farm productivity by dim<strong>in</strong>ish<strong>in</strong>g shrimp growth<br />
and/or promot<strong>in</strong>g shrimp disease outbreaks (Hargreaves, 1998; L<strong>in</strong>, 1989).<br />
Identify<strong>in</strong>g <strong>aquaculture</strong> species and system that are expected to be profitable is an<br />
essential step toward develop<strong>in</strong>g susta<strong>in</strong>able <strong>aquaculture</strong> and to decrease the<br />
adverse impact (Andersen, 2002 <strong>in</strong> Leung et al., 2007). Asian countries have been<br />
practic<strong>in</strong>g polyculture <strong>systems</strong>, through trial and error and experimentation for<br />
centuries (Qian et al., 1996). These strategies were motivated by the need to<br />
maximize productivity per unit of land and water bodies. They were based on<br />
diversified self-reliance <strong>in</strong> feed and basic raw material production and the<br />
philosophy that the by-products (wastes) from one resource use must become an<br />
<strong>in</strong>put of another resource <strong>in</strong> use (Chop<strong>in</strong> et al., 2001; Neori et al., 2004). On the<br />
other hand polyculture has disadvantage as it could decrease ma<strong>in</strong> target<br />
organisms production due to competition <strong>in</strong> space and <strong>nutrient</strong> utilization with cocultured<br />
organisms.<br />
Shrimp Penaeus vannamei, seaweed Gracillaria verrucosa and fish Oreochromis<br />
sp. had been used <strong>in</strong> presented thesis due to the different trophic level they<br />
<strong>in</strong>habitated, the high economic value, and well developed knowledge of<br />
cultivation. Hypothesis of this study are: (1) <strong>nutrient</strong> given to the ponds can be<br />
used most efficiently by polyculture system, (2) polyculture system us<strong>in</strong>g shrimp,<br />
seaweed and fish can be used to m<strong>in</strong>imize adverse impact of <strong>aquaculture</strong> to the<br />
environment, (3) seaweed Gracillaria verrucosa can be used to absorb <strong>nutrient</strong><br />
excretion from shrimp and fish wastes and may contribute to the oxygen budget.<br />
2
To prove this hypothesis, <strong>in</strong> Chapter 1 of present study, based on a literature<br />
review polyculture system can be described as the practice of cultur<strong>in</strong>g more than<br />
one aquatic organism <strong>in</strong> the same system. In Chapter 2, empiricial calculations of<br />
<strong>nutrient</strong>s <strong>fluxes</strong> and mass balances <strong>in</strong> monoculture and polyculture <strong>systems</strong> with<br />
shrimp Penaeus vannamei and seaweed Gracillaria verrucosa were realized and<br />
compared. Additional <strong>in</strong>vestigations were conducted <strong>in</strong> Chapter 3 to determ<strong>in</strong>e<br />
<strong>nutrient</strong> <strong>fluxes</strong> and mass balances <strong>in</strong> various polyculture <strong>systems</strong> us<strong>in</strong>g shrimp<br />
Penaeus vannamei, Fish Oreochromis sp. and Seaweed Gracillaria verrucosa.<br />
F<strong>in</strong>ally, <strong>in</strong> Chapter 4, nitrogen assimilation potential of seaweed Gracillaria<br />
verrucosa <strong>in</strong> polyculture with pacific white shrimps Penaeus vannamei was<br />
estimated.<br />
References<br />
Boyd, C. E. 1999. Codes of Practise for Responsible Shrimp Farm<strong>in</strong>g. Global<br />
Aquaculture Alliance. St. Louis MO. USA. 48.<br />
Chop<strong>in</strong>, T., A. H Buschmann, C. Hall<strong>in</strong>g, M Troell, N Kautsky, A. Neori, G.<br />
Kraemer, J. Zertuche-Gonzalez, C. Yarish, C. Neefus. 2001. Integrat<strong>in</strong>g<br />
seaweeds <strong>in</strong>to <strong>aquaculture</strong> <strong>systems</strong>: a key towards susta<strong>in</strong>ability. J Phycol<br />
37:975–986.<br />
FAO. 2010. The state of world fisheries and <strong>aquaculture</strong>. Fisheries and<br />
<strong>aquaculture</strong> department. Food and Agriculture Organization of United<br />
Nations. Rome. Italy.<br />
Hargreaves, J.A. (1998). Nitrogen biogeochemistry of <strong>aquaculture</strong> ponds.<br />
Aquaculture 166, 181–212.<br />
Neori, A., T. Chop<strong>in</strong> T, M. Troell, A. H. Buschmann, G.P. Kraemer, C. Hall<strong>in</strong>g,<br />
M. Shpigel, C Yarish. 2004. Integrated <strong>aquaculture</strong>: rationale, evolution<br />
and state of the art emphasiz<strong>in</strong>g seaweed biofiltration <strong>in</strong> modern<br />
mariculture. Aquaculture 231:361–391.<br />
Pearson, T. H., and R. J. Gowen. 1990. Impact of caged fish farm<strong>in</strong>g on the<br />
mar<strong>in</strong>e environment – the Scottisch experience, 9-13. In <strong>in</strong>teractions<br />
between <strong>aquaculture</strong> and the environment, vol. An Taisce - The National<br />
Trust for Ireland, Dubl<strong>in</strong>.<br />
3
Troell M, C. Hall<strong>in</strong>g, A. Neori, T. Chop<strong>in</strong>, A. H. Buschmann, N. Kautsky, C.<br />
Yarish. 2003. Integrated mariculture: ask<strong>in</strong>g the right questions.<br />
Aquaculture 226:69–90.<br />
Qian, P. Y., C. Y. Wu, M. Wu, Y. K. Xie. 1996. Integrated cultivation of red alga<br />
Kappaphycus alvarezii and the pearl oyster P<strong>in</strong>ctada martensi.<br />
Aquaculture 147: 21-35<br />
4
Chapter 1: Nutrient Flux <strong>in</strong> Polyculture System Us<strong>in</strong>g Seaweed as<br />
Biofilter: Implications for Susta<strong>in</strong>ability (M<strong>in</strong>i Review)<br />
Y. N. Ihsan ab , K. J. Hesse c , C. Schulz ab<br />
a Gesellschaft <strong>für</strong> Mar<strong>in</strong>e Aquakultur mbH, Hafentörn 3, D-25761 Büsum<br />
b <strong>Institut</strong>e for Animal Breed<strong>in</strong>g and Husbandry, Christian-Albrechts-Universität<br />
D-24098 Kiel<br />
c Research and Technology Centre, Christian-Albrechts-Universität<br />
D-25761 Büsum<br />
Submitted to the Journal of Asian Fisheries Society<br />
5
Abstract<br />
In general, feed based shrimp and fish <strong>aquaculture</strong> can produce a large amount of<br />
waste, <strong>in</strong>clud<strong>in</strong>g nitrogen and phosphorus that is released to the aquatic<br />
environment without treatment. One of the ma<strong>in</strong> environmental issues is the direct<br />
discharge of significant <strong>nutrient</strong> loads <strong>in</strong>to coastal waters from <strong>aquaculture</strong> ponds<br />
system. In its search for best management practices, the <strong>aquaculture</strong> <strong>in</strong>dustry<br />
should develop <strong>in</strong>novative and responsible practices that optimize its efficiency<br />
and create diversification, while ensur<strong>in</strong>g the remediation of the consequences of<br />
its activities to ma<strong>in</strong>ta<strong>in</strong> the health of coastal waters. At present, seaweed<br />
cultivation <strong>in</strong> <strong>in</strong>tegrated polyculture system appears to be a viable approach to<br />
reduce discharge <strong>nutrient</strong>s to the environment. By <strong>in</strong>tegrat<strong>in</strong>g fed <strong>aquaculture</strong>, the<br />
wastes of one resource user become a resource for the others (Neori et al., 2004).<br />
Seaweed can be efficient at removal of <strong>nutrient</strong>s from effluent of <strong>in</strong>tensive fish<br />
farm (Troell et al., 1997; Neori et al., 2004). The production of seaweed <strong>in</strong> cage<br />
culture can be successfully <strong>in</strong>tegrated with production of fish and shrimp.<br />
Regard<strong>in</strong>g the environmental benefits of <strong>in</strong>tegrated seaweed and fish or shrimp<br />
production, seaweed culture can also benefit by <strong>in</strong>creas<strong>in</strong>g their economic<br />
viability. Integrated seaweed <strong>aquaculture</strong> <strong>systems</strong> have been suggested as a<br />
possible solution for secur<strong>in</strong>g an <strong>in</strong>creas<strong>in</strong>g and environmentally sounded<br />
production of future supply of fish and seafood.<br />
6
Introduction<br />
Aquaculture has expanded rapidly all over of the world, especially <strong>in</strong> tropical<br />
areas which account for 89% of production <strong>in</strong> terms of quantity and 79% <strong>in</strong> terms<br />
of value (FAO, 2010). Aquaculture production (exclud<strong>in</strong>g seaweed) was less than<br />
1 million tons per year <strong>in</strong> the early 1950, production <strong>in</strong> 2008 already achieved<br />
52.5 million tons, with a value of US$ 98.4 billion. Seaweed production by<br />
<strong>aquaculture</strong> <strong>in</strong> 2008 was 15.8 million tons (live weight equivalent), with a value<br />
of US$7.4 billion, represent<strong>in</strong>g an average annual growth rate <strong>in</strong> terms of weight<br />
of almost 8% s<strong>in</strong>ce 1970. If seaweed is <strong>in</strong>cluded, total global <strong>aquaculture</strong><br />
production <strong>in</strong> 2008 amounted to 68.3 tons with a first-sale value of US$ 106<br />
billion (FAO, 2010). It is expected that world <strong>aquaculture</strong> production will<br />
cont<strong>in</strong>ue to grow <strong>in</strong> the com<strong>in</strong>g decade. Aquaculture is a source of <strong>in</strong>come and<br />
livelihood for millions of people around the world. Employment <strong>in</strong> fisheries and<br />
<strong>aquaculture</strong> has grown substantially <strong>in</strong> the last three decades, with an average rate<br />
of <strong>in</strong>crease of 3.6% per year s<strong>in</strong>ce 1980 (FAO, 2010).<br />
The expansion of <strong>aquaculture</strong> has brought concern about the possible effect of<br />
<strong>aquaculture</strong> effluents on coastal ecosystem. Aquaculture has contributed to<br />
environment degradation, with visible effect such as <strong>in</strong>creases <strong>in</strong> particulate<br />
organic matter and chemical change such as dissolved oxygen reduction and<br />
<strong>in</strong>creased nitrogen and phosphorus concentrations <strong>in</strong> water (Troell et al., 1999).<br />
The negative impact of <strong>aquaculture</strong> on the environment due to the release of<br />
nitrogen and phosphorus is related to eutrophication processes, especially <strong>in</strong><br />
coastal and sheltered areas (Neori et al., 2000; Neori and Shpigel, 2003). This<br />
<strong>nutrient</strong> release is primarily caused by <strong>in</strong>tensive and semi <strong>in</strong>tensive production of<br />
fish. Feed and fertilizer which are applied <strong>in</strong> ponds are not fully <strong>in</strong>corporated <strong>in</strong>to<br />
the cultured species partly deposited <strong>in</strong> pond sediments or discharged as effluents.<br />
In average, fish or shrimp assimilates only 23-31% of nitrogen and 10-13% of<br />
phosphorus of the total <strong>in</strong>puts and rema<strong>in</strong><strong>in</strong>g 14-53% of nitrogen and 39-67% of<br />
phosphorus are deposited <strong>in</strong> the sediment (Neori et al., 2000; Dhirendra and L<strong>in</strong>,<br />
2002; Schuenhoff et al., 2003). Nutrient <strong>in</strong> <strong>aquaculture</strong> effluents are distributed <strong>in</strong><br />
a particulate or soluble fraction (Ackefors and Enell, 1994). In fresh manure,<br />
about 7-32% of total nitrogen (TN) and 30-84% of total phosphorus (TP) are<br />
7
ound <strong>in</strong> this particulate fraction and the rema<strong>in</strong>der are excreted <strong>in</strong> dissolved<br />
forms (Bergheim et al., 1993). In <strong>in</strong>tensive mar<strong>in</strong>e shrimp culture, only 24% and<br />
13% of dietary nitrogen and phosphorus were <strong>in</strong>corporated <strong>in</strong>to harvested shrimp,<br />
while the rema<strong>in</strong><strong>in</strong>g <strong>nutrient</strong>s were released <strong>in</strong>to the surround<strong>in</strong>g water (Briggs<br />
and Funge-Smith, 1994). Phosphorus releases were estimated to be 9.4 kg<br />
(Ackefors and Enell, 1990) and 19.6–22.4 kg (Holby and Hall, 1991) per ton of<br />
shrimp produced. This release may cause environmental and socio-economic<br />
problems (Troell et al., 1999). The future <strong>aquaculture</strong> must be based on the<br />
development of susta<strong>in</strong>able environmentally sounded production techniques<br />
(Neori et al., 2004).<br />
In recent years, <strong>in</strong>tegrated <strong>aquaculture</strong> has been proposed as a mean to reduce the<br />
<strong>nutrient</strong> load<strong>in</strong>g from <strong>aquaculture</strong>, <strong>in</strong>clud<strong>in</strong>g the improvement of feed utilization<br />
by animals. Feed <strong>aquaculture</strong> (e.g. f<strong>in</strong>fish, shrimp) needs to be <strong>in</strong>tegrated with<br />
organic and <strong>in</strong>organic extractive <strong>aquaculture</strong> (e.g. shellfish and seaweed). Schulz<br />
et al. (2003) reported the total suspended solids (TSS) were reduced by 95.8-<br />
97.3% from ra<strong>in</strong>bow trout farm effluent <strong>in</strong> constructed wetland with emergent<br />
plants and subsurface horizontal water flow. This <strong>nutrient</strong> <strong>in</strong>corporation of cocultured<br />
organisms of different trophic levels is the basis of environmentally<br />
sounded <strong>aquaculture</strong> (Chop<strong>in</strong> et al., 2001; Neori et al., 2004). Integrated<br />
<strong>aquaculture</strong> provides <strong>nutrient</strong> bioremediation, mutual benefits to the co-cultured<br />
organisms, economic diversification and <strong>in</strong>creased profitability. Ideally, <strong>nutrient</strong><br />
process <strong>in</strong> polyculture system with two or more ecologically compatible species<br />
should be balanced, waste from one species are recycled as fertilizer or feed by<br />
another without conflict<strong>in</strong>g with each other (Neori et al., 2000).<br />
The aim of this paper is to present and discuss the <strong>nutrient</strong> <strong>fluxes</strong> from various<br />
polyculture <strong>systems</strong> on coastal waters. Additionally, comparative studies <strong>in</strong> this<br />
paper provide evidence that polyculture represents a promis<strong>in</strong>g technique relative<br />
to conventional monoculture for the production of <strong>aquaculture</strong>.<br />
Polyculture system<br />
Polyculture is the practice of cultur<strong>in</strong>g more than one species of aquatic organism<br />
<strong>in</strong> the same pond. The motivat<strong>in</strong>g pr<strong>in</strong>ciple is that fish production <strong>in</strong> ponds may<br />
8
e maximized by rais<strong>in</strong>g a comb<strong>in</strong>ation of species hav<strong>in</strong>g different food habits.<br />
The concept of polyculture of fish is based on the concept of total utilization of<br />
different trophic and spatial niches of a pond <strong>in</strong> order to obta<strong>in</strong> maximum fish<br />
production per unit area (Edward, 1992; Chiang, 1993; Qian et al., 1996). The<br />
mixture of fish gives better utilization of available natural food produced <strong>in</strong> a<br />
pond. The compatible fish species hav<strong>in</strong>g complimentary feed<strong>in</strong>g habits are<br />
stocked so that all the ecological niches of pond ecosystem are effectively<br />
utilized. The possibility of <strong>in</strong>creas<strong>in</strong>g fish production per unit area, through<br />
polyculture, is considerable, when compared with monoculture system of fish.<br />
Different species comb<strong>in</strong>ation <strong>in</strong> polyculture system effectively contributes also to<br />
improve the pond environment (Buschmann, 1996; Schuenhoff et al., 2003; Matos<br />
et al., 2006).<br />
Ponds that have been enriched through chemical fertilization, manur<strong>in</strong>g or feed<strong>in</strong>g<br />
practices conta<strong>in</strong> abundant natural fish food organisms liv<strong>in</strong>g at different depths<br />
and locations <strong>in</strong> the water column. Most fish feed predom<strong>in</strong>antly on selected<br />
groups of these organisms. Polyculture should comb<strong>in</strong>e fish hav<strong>in</strong>g different<br />
feed<strong>in</strong>g habits <strong>in</strong> proportions that effectively utilize these various natural feed<br />
items (Figure 1). As a result, higher yields are obta<strong>in</strong>ed (Bocek, unpublished).<br />
Figure 1: Polyculture utilizes natural foods efficiently<br />
(source: Bocek, unpublished)<br />
9
Shrimp ponds are traditionally set up <strong>in</strong> mar<strong>in</strong>e coastal areas and can lead to<br />
adverse impact on the environment, especially of large areas of mangrove forest.<br />
Cage culture can be a more susta<strong>in</strong>able alternative for rear<strong>in</strong>g shrimp and<br />
polyculture with seaweed may also improve susta<strong>in</strong>ability.<br />
Table 1. Worldwide polyculture system<br />
Species Location Objective References<br />
Shrimp (Penaeus monodon)<br />
and Milkfish (Chanos<br />
chanos)<br />
Abalone (Haliotis<br />
tuberculata), fish, and<br />
seaweed (Ulva lactuca)<br />
Thailand To compare shrimp<br />
performance<br />
between mono and<br />
polyculture system<br />
Israel To evaluated Nbudgets<br />
and fish<br />
performance<br />
Tilapia and shrimp Thailand To <strong>in</strong>crease fish<br />
production<br />
Fish (Sparus aurata and<br />
seaweed (Ulva. lactuca)<br />
Shrimp (Litopenaeus<br />
vannamei) and seaweed<br />
(Kappaphycus alvarezii)<br />
Portugal To evaluated the<br />
performance of<br />
ponds with effluent<br />
through seaweed<br />
Brazil To test the<br />
feasibility of cocultur<strong>in</strong>g<br />
shrimp<br />
and seaweed<br />
Kuntiyo and Balio,<br />
1997<br />
Neori et al., 1998<br />
Yi et al., 2003<br />
Schuenhoff et al.,<br />
2003<br />
Lombardi et al.,<br />
2006<br />
Table 1 show the worldwide various polyculture <strong>systems</strong> that have been done by<br />
several researchers. Kuntiyo and Balio (1997) reported after 109 culture days,<br />
results showed no significant difference (P>0.05) on growth and survival rates of<br />
both commodities <strong>in</strong> two culture schemes. Mean weight ga<strong>in</strong> was 30.88 g for<br />
shrimp and 263.33 g for milkfish <strong>in</strong> monoculture and 31.85 g and 210.57 g for<br />
shrimp and milkfish, respectively, <strong>in</strong> the polyculture system. Mean survival rates<br />
10
were 94.03% for shrimp and 99.0% for milkfish <strong>in</strong> monoculture; and 82.13% for<br />
shrimp and 92.33% for milk-fish for the polyculture system. Net aggregate<br />
production, however, was highly significant <strong>in</strong> polyculture, atta<strong>in</strong><strong>in</strong>g 923.50<br />
kg/ha/crop. Economic feasibility revealed encourag<strong>in</strong>g results for polyculture over<br />
monoculture, with return on <strong>in</strong>vestment (ROI) valued at 45% for polyculture.<br />
Nutrient flux<br />
The two significant components of the pond environment are the pond water and<br />
sediment which <strong>in</strong>teract cont<strong>in</strong>uously to <strong>in</strong>fluence the culture environment. Pond<br />
sediment can be further divided <strong>in</strong>to the pond soil component (the pond bottom<br />
and walls) and the accumulated sediment component (Briggs and Funge-Smith,<br />
1994).<br />
Nutrient budget are derived for solid, particulate organic matter, nitrogen, and<br />
phosphorus. The erosion of pond soil is the major source of solid budget and<br />
organic matter <strong>in</strong> the pond. The feed applied to the pond is a significant source of<br />
organic matter (31-50%) <strong>in</strong> the pond but contributed little amount of solids (4-7%)<br />
to the system (Funge-Smith and Briggs, 1998). This is important s<strong>in</strong>ce the feed<br />
component is also an <strong>in</strong>dication of the faecal contribution by fish or shrimp.<br />
Funge-Smith and Stewart (1996) reported the nitrogen budgets reveal <strong>in</strong> more<br />
detail, the source and s<strong>in</strong>ks of the organic components <strong>in</strong> an <strong>in</strong>tensive shrimp pond<br />
(Table 2). Applied feed accounted for 78% of the <strong>in</strong>put N to the ponds. Erosion of<br />
the pond soils, whilst a major contributor of solid, accounted for only 16% of<br />
added to the system. Other m<strong>in</strong>or contribution was <strong>in</strong>fluent water (4.03%), and<br />
fertilizer, ra<strong>in</strong>fall, shrimp stocked (2%). The s<strong>in</strong>ks for nitrogen were the sediments<br />
(24%), harvested shrimp (18%), and discharged water (28%). This leaves<br />
approximately 30% of the nitrogen unaccounted for which is assumed to be N lost<br />
to the atmosphere as N2.<br />
11
Table 2. Nitrogen budget for <strong>in</strong>tensive shrimp ponds (Funge-Smith and Stewart,<br />
1996)<br />
Source and s<strong>in</strong>ks Nitrogen (%)<br />
Nitrogen <strong>in</strong>put<br />
Feed 78<br />
Fertilizer 1.8<br />
Ra<strong>in</strong>fall 0.12<br />
Shrimp stocked 0.02<br />
Influent water 4.03<br />
Erosion of pond soil 16<br />
Nitrogen output<br />
Sediment removal 24<br />
Shrimp harvest 18<br />
Water outflow 17<br />
Harvest dra<strong>in</strong>age 11<br />
Denitrification 30<br />
Application of seaweed to polyculture system<br />
The use of seaweed <strong>in</strong>tegrated with fish cultures has been studied <strong>in</strong> open water<br />
and land-based system condition <strong>in</strong> Israel, Portugal, Brazil, and Indonesia (Neori<br />
et al., 1998; Schuenhoff et al., 2003; Lombardi et al., 2006). General concepts<br />
about <strong>nutrient</strong> uptake by seaweed can be found <strong>in</strong> Harrison and Hurd (2001). To<br />
optimize the seaweed component of an <strong>in</strong>tegrated <strong>aquaculture</strong> system, particular<br />
attention should be given not only to physical and chemical factors such as light,<br />
temperature, effluent <strong>nutrient</strong> concentration and flux, and water motion but also<br />
biological factors such as <strong>in</strong>terplant variability, <strong>nutrient</strong> prehistory, type of plant<br />
tissue and age.<br />
A pilot scale system for the <strong>in</strong>tensive abalone <strong>in</strong> polyculture system was<br />
established aimed at elim<strong>in</strong>at<strong>in</strong>g the dependence on external feed source and<br />
<strong>nutrient</strong> discharge levels. Effluents from abalone (Haliotis tuberculata) culture<br />
tanks dra<strong>in</strong>ed <strong>in</strong>to seaweed (Ulva lactuca) culture and biofilter tanks. Nitrogenous<br />
12
waste products by abalone contributed to the nutrition of seaweed. The abalone<br />
grew on average 0.26%/d and mean seaweed production amounted 230 g/m 2 /d.<br />
Nitrogen supplied was removed on average 58% (Neori et al., 1998).<br />
Polyculture system consisted of fish and seaweed was evaluated by Schuenhoff et<br />
al. (2003). An <strong>in</strong>tensive fishpond (Sparus aurata) and three stage seaweed Ulva<br />
lactuca biofilter were used which recirculated 50% of the effluent back to the<br />
fishpond. Seaweed mean production was 94 g/m 2 /day. Nitrogen content of Ulva<br />
lactuca was 34% of dry weight. Seaweed Ulva lactuca can remove 30% of<br />
dissolved <strong>nutrient</strong> load from fishpond.<br />
There were no negative <strong>in</strong>terferences <strong>in</strong> co-cultur<strong>in</strong>g shrimp and seaweed <strong>in</strong>side<br />
the same cage. Lombardi et al. (2006) reported no significant difference (P>0.05)<br />
between two treatment (monoculture and polyculture with seaweed) for shrimp<br />
weight ga<strong>in</strong>, food conversion rate (FCR), and survival rate. Shrimp yield reached<br />
production rates of 3.23 kg/m 2 /a and seaweed Kappaphycus alvarezii production<br />
reached rates as high as 23.70 kg/m 2 /a. It means seaweed is able to grow <strong>in</strong>side<br />
shrimp cage (Table 3).<br />
Seaweed can also be a useful tool for measur<strong>in</strong>g the zone of <strong>in</strong>fluence of an<br />
<strong>aquaculture</strong> site, because they are <strong>in</strong>tegrators of bioavailable <strong>nutrient</strong>s over time<br />
(Troell et al., 1997). Jimenez del Rio (1994) found that <strong>in</strong>creas<strong>in</strong>g ammonium<br />
load<strong>in</strong>g rates per unit area of Ulva lactuca tank cultures fed with fish effluents led<br />
to decrease dissolved nitrogen efficiency but <strong>in</strong>creased nitrogen area uptake rate.<br />
Seaweed yield and prote<strong>in</strong> content also <strong>in</strong>creased with <strong>in</strong>creas<strong>in</strong>g ammonium<br />
supply per unit area. The same conclusion as ammonium uptake efficiency<br />
decreased with the water turnover rate but the uptake per gram of Gracillaria per<br />
time <strong>in</strong>creased (Troell et al., 1997). Seaweed performs better as nitrogen absorber<br />
with ammonium than with nitrate which is excellent <strong>in</strong> context on <strong>in</strong>tensive fish<br />
<strong>aquaculture</strong> where most of nitrogen is released as ammonium (Carmona et al.,<br />
2001).<br />
Review of result<br />
Polyculture <strong>systems</strong> us<strong>in</strong>g seaweeds for the removal or conversion of wastes has<br />
been done together with shrimp or fish. Lombardi et al. (2006) calculated the<br />
13
mean relative growth rate (RGR) for seaweed is 0.80-1.30%/day. This value is<br />
lower compared to the others (Table 3). The highest RGR is nearly 3.00%/day<br />
reported by Eswaran et al. (2002). The result suggest that depth is the ma<strong>in</strong> factor<br />
that affects the growth of seaweed, because <strong>in</strong> most of the experiment higher RGR<br />
were observed on surface float<strong>in</strong>g ropes, whereas the lowest RGR from Lombardi<br />
et al. (2006) were cultured at different depth between 1 – 2 m.<br />
Table 3. Relative growth rate (RGR) of seaweed <strong>in</strong> various studies (Lombardo et<br />
al., 2006)<br />
RGR (%) Condition Reference<br />
0.80 – 1.30 Inside cages Lombardy et al., 2006<br />
3.72 – 7.17 Inside cages Hurtado-Ponce, 1992<br />
8.00 – 10.00 Outside cages R<strong>in</strong>cones and Rubio,<br />
1998<br />
4.00 – 8.00 Outside cages Ohno et al., 1999<br />
2.30 – 4.20 Outside cages Hurtado et al., 2001<br />
6.50 – 10.70 Outside cages De Paula et al., 2001<br />
Nearly 3.00 Outside cages Eswaran et al., 2002<br />
Dur<strong>in</strong>g the last decade, renewed <strong>in</strong>terest <strong>in</strong> <strong>in</strong>corporat<strong>in</strong>g seaweed as a biofilter<br />
l<strong>in</strong>k <strong>in</strong> <strong>in</strong>tegrated carnivore-herbivore polyculture system has produce new<br />
approach and practical technologies (Troell et al., 1999; De Paula et al., 2002;<br />
Eswaran et al., 2002; Lombardi et al., 2006). These studies <strong>in</strong>dicate that seaweeds<br />
especially Gracillaria sp. can assimilate as much as 5-20% of the ammonium<br />
produced by <strong>in</strong>tensive fish or shrimp culture (Lombardi et al., 2006).<br />
The ma<strong>in</strong> issue <strong>in</strong> the effective implementation of polyculture <strong>systems</strong> is their<br />
optimal function<strong>in</strong>g, which requires an <strong>in</strong>-depth understand<strong>in</strong>g of the physiology<br />
and nutrition of the selected species. With seaweed, like with many organisms, the<br />
different physiological processes tak<strong>in</strong>g place have different environmental<br />
requirements (Harrison and Hurd, 2001). Consequently, the optimization of the<br />
overall efficiency of a cultivation system can be complex because it will require a<br />
compromise between apparently conflict<strong>in</strong>g objective e.g. biomass or particular<br />
14
compound production versus bioremediation efficiency (Chop<strong>in</strong> and Yarish,<br />
1998). For example, growth, <strong>nutrient</strong> uptake, carrageenan (agar production), and<br />
phycocolloid quality respond differentially to <strong>nutrient</strong> enrichment (Buschmann et<br />
al., 2001).<br />
In tank culture, <strong>nutrient</strong> availability can be controlled by chang<strong>in</strong>g the water flow.<br />
By <strong>in</strong>creas<strong>in</strong>g the water flow, <strong>nutrient</strong> flux will <strong>in</strong>crease as well, which allows a<br />
high biomass production of <strong>nutrient</strong>-sufficient seaweeds. In the other side, the<br />
<strong>nutrient</strong> uptake efficiency is low and <strong>nutrient</strong> concentration rema<strong>in</strong>s high <strong>in</strong> the<br />
effluents. If the water flow is low, <strong>nutrient</strong>s become limit<strong>in</strong>g and seaweed biomass<br />
production decreases, but the <strong>nutrient</strong> uptake efficiency is higher (Hanisak, 1998).<br />
If seaweed is only used as a biofilter and identified low commercial value species<br />
like Ulva lactuca, they can be used to depurate fish effluents (Schuenhoff et al.,<br />
2003). However, this apparent bioremediation merely shifts the problem of waste<br />
disposal as the seaweed scrubber will <strong>in</strong> turn need to be disposed of or treated. On<br />
the other hand, species like Gracilaria sp., Porphyra sp., or Lam<strong>in</strong>aria sp. offer<br />
both high bioremediation efficiency and commercial value <strong>in</strong> established market<br />
such as human consumption (Neori and Shpigel, 1999).<br />
When the value added for the service of improv<strong>in</strong>g water quality and coastal<br />
health is f<strong>in</strong>ally recognized, quantified and comb<strong>in</strong>ed with that of the pr<strong>in</strong>cipal<br />
crop (shrimp <strong>aquaculture</strong>), the seaweed component of a polyculture system will be<br />
understood to significantly improve the success of a diversified operation. An<br />
accrued benefit to operators of polyculture system is the fact that the currently<br />
discharge (unassimilated or excreted) nitrogen and phosphorus, which represent a<br />
loss of money <strong>in</strong> real terms, will be captured and converted <strong>in</strong>to the production of<br />
salable biomass and bioproducts, hence generat<strong>in</strong>g revenues that may more than<br />
compensate for the expenses. Additionally, as legislative guidel<strong>in</strong>es, standards,<br />
and controls regard<strong>in</strong>g the discharge of <strong>in</strong>organic <strong>nutrient</strong>s <strong>in</strong>to coastal waters<br />
become more str<strong>in</strong>gent <strong>in</strong> many countries and for susta<strong>in</strong>able <strong>aquaculture</strong>,<br />
bioremediation via the production of seaweeds will help the shrimp <strong>aquaculture</strong><br />
<strong>in</strong>dustry and avoid noncompliance.<br />
To successfully develop <strong>in</strong>tegrated <strong>aquaculture</strong> system, much research and<br />
development rema<strong>in</strong>s to be undertaken, particularly <strong>in</strong> the follow<strong>in</strong>g areas:<br />
15
1. Transfer and modification of cultivation technologies to local environments<br />
and socioeconomics,<br />
2. development of the cultivation of native species of marketable value that will<br />
be fast grow<strong>in</strong>g at different times of the year and <strong>in</strong> diverse habitats,<br />
3. site-specific biological, chemical, physical, and socioeconomic modell<strong>in</strong>g to<br />
def<strong>in</strong>e the appropriate proportions between the different co-cultured<br />
organisms.<br />
Conclusions<br />
Responsible <strong>aquaculture</strong> practices should be based on balanced ecosystem<br />
management approach, the basic premise of which is to <strong>in</strong>corporate the biological<br />
and environmental function of a diverse group of organisms <strong>in</strong>to a unified system<br />
that ma<strong>in</strong>ta<strong>in</strong>s the natural <strong>in</strong>teraction of species and allows an ecosystem to<br />
function susta<strong>in</strong>ably. To help and to ensure its susta<strong>in</strong>ability, however, it needs to<br />
responsibly change its too often monoculture practices by adopt<strong>in</strong>g polyculture<br />
ones to become better <strong>in</strong>tegrated <strong>in</strong>to broader coastal management framework.<br />
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carrageenophyte Kappaphycus alvarezii (Rhodophyta, Gigart<strong>in</strong>ales)<br />
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Hanisak, M. D. 1998. Seaweed cultivation: global trends. World Aquaculture,<br />
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de Paula, E. J. 2006. Cage polyculture of the Pacific white shrimp<br />
Litopenaeus vannamei and the Philipp<strong>in</strong>es seaweed Kappaphycus<br />
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Neori, A., Ragg, N. L.C., Shpigel, M. 1998. The <strong>in</strong>tegrated culture of seaweed,<br />
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Neori, A., M Shpigel, D. Ben-Ezra. 2000. Susta<strong>in</strong>able <strong>in</strong>tegrated system for<br />
culture fish, seaweed and abalone. Aquaculture. 186. 279-291.<br />
Neori, A., T. Chop<strong>in</strong> T, M. Troell, A. H. Buschmann, G.P. Kraemer, C. Hall<strong>in</strong>g,<br />
M. Shpigel, C Yarish. 2004. Integrated <strong>aquaculture</strong>: rationale, evolution<br />
and state of the art emphasiz<strong>in</strong>g seaweed biofiltration <strong>in</strong> modern<br />
mariculture. Aquaculture 231:361–391.<br />
Neori, A. and Shpigel, M. 2003. Us<strong>in</strong>g algae to treat effluents and feed<br />
<strong>in</strong>vertebrates <strong>in</strong> susta<strong>in</strong>able <strong>in</strong>tegrated mariculture. World Aquacult<br />
30(2):46–51<br />
Schuenhoff, A., Shpigel, M., Lupatsch, I., Ashkenazi, A., Msuya, F. E., Neori, A.<br />
2003. A semi-recirculat<strong>in</strong>g, <strong>in</strong>tegrated system for the culture of fish and<br />
seaweed. Aquaculture 221:167–181.<br />
18
Schulz, C., J. Gelbrecht, B. Rennert. 2003. Treatment of ra<strong>in</strong>bow trout farm<br />
effluents <strong>in</strong> constructed wetland with emergent plants and subsurface<br />
horizontal water flow. Aquaculture. Elsevier. 217: 207-221.<br />
Troell, M., C Hall<strong>in</strong>g, A Nilsson, A. H Buschmann., N Kautsky, L Kautsky. 1997.<br />
Integrated mar<strong>in</strong>e cultivation of Gracillaria chilensis (Gracilariales,<br />
Bangiophyceae) and salmon cages for reduced environmental impact and<br />
<strong>in</strong>creased economic output. Aquaculture 156:45–61.<br />
Troell, M., P. Ronnback, C. Hall<strong>in</strong>g, N. Kautsky and A.H. Buschmann. 1999.<br />
Ecological eng<strong>in</strong>eer<strong>in</strong>g <strong>in</strong> <strong>aquaculture</strong>: Use of seaweeds for remov<strong>in</strong>g the<br />
<strong>nutrient</strong>s from the <strong>in</strong>tensive mariculture. J. Appl. Phycol., 11: 89-97.<br />
19
Chapter 2: A Comparison of Nutrients Fluxes <strong>in</strong> Monoculture and<br />
Polyculture Systems for Shrimp (Penaeus vannamei) and<br />
Seaweed (Gracillaria verrucosa) Production<br />
Y. N. Ihsan ab , K. J. Hesse c , N. Holmgren d, C. Schulz ab<br />
a Gesellschaft <strong>für</strong> Mar<strong>in</strong>e Aquakultur mbH, Hafentörn 3, D-25761 Büsum<br />
b <strong>Institut</strong>e for Animal Breed<strong>in</strong>g and Husbandry, Christian-Albrechts-Universität<br />
D-24098 Kiel<br />
c Research and Technology Centre, Christian-Albrechts-Universität<br />
D-25761 Büsum<br />
d<br />
University of Skövde – Sweden<br />
541 28, Skövde – Sweden<br />
Submitted to the Journal of World Aquaculture Society<br />
20
Abstract<br />
Integrated <strong>aquaculture</strong> <strong>systems</strong> are well known to utilize various forms of<br />
<strong>nutrient</strong>s with higher total assimilation rates than monoculture. In order to<br />
evaluate the <strong>nutrient</strong> efficiency of comb<strong>in</strong>ed shrimp and seaweed production<br />
<strong>nutrient</strong> <strong>fluxes</strong> were compared with shrimp monoculture <strong>systems</strong>. Therefore<br />
triplicate ponds of 1200 m² were stocked with Gracillaria verrucosa (50 kg) and<br />
20 <strong>in</strong>dividuals of shrimp (0.22 ± 0.016 g/<strong>in</strong>d)/m 2 . The culture period lasted 100<br />
days and water samples to describe <strong>nutrient</strong> <strong>fluxes</strong> were taken every 10 days. The<br />
average ammonium-nitrogen concentration over the whole period was 0.24 mg/l<br />
<strong>in</strong> polyculture while <strong>in</strong> monoculture 0.37 mg/l of ammonium-nitrogen were<br />
analyzed. Survival rate of shrimp <strong>in</strong> polyculture and monoculture were 86.32%<br />
and 69.17% respectively. A mass balance model was developed for total nitrogen<br />
and total phosphorus to estimate their <strong>fluxes</strong>. From the total nitrogen and total<br />
phosphorus <strong>in</strong>put, 24.2% and 5.3% were <strong>in</strong>corporated <strong>in</strong> 335.7 kg/1200 m 2 shrimp<br />
weight ga<strong>in</strong> <strong>in</strong> monoculture, while 30.8% and 6.9% were <strong>in</strong>corporated <strong>in</strong> 501.5<br />
kg/1200m 2 shrimp weight ga<strong>in</strong> and 3.5% and 2.4% were <strong>in</strong>corporated <strong>in</strong> 325<br />
kg/1200 m 2 seaweed Gracillaria <strong>in</strong> polyculture system. Therefore, polyculture<br />
<strong>systems</strong> us<strong>in</strong>g seaweed Gracillaria seem to act more efficiently with regard to<br />
<strong>nutrient</strong> accumulation.<br />
21
Introduction<br />
Shrimp <strong>aquaculture</strong> has been developed towards a commercial <strong>in</strong>dustry <strong>in</strong><br />
Southeast Asian countries <strong>in</strong>clud<strong>in</strong>g Indonesia. The coastal area, which <strong>in</strong>cludes<br />
mangrove forests, has been changed to be utilized for <strong>aquaculture</strong> activities with<strong>in</strong><br />
the last decades (Clough, 1993). Moreover, an effluent conta<strong>in</strong><strong>in</strong>g a large quantity<br />
of <strong>nutrient</strong>s as a result of feed and fertilizer application, has been discharged from<br />
<strong>aquaculture</strong> ponds <strong>in</strong>to the environment. Rapid development of <strong>in</strong>tensive<br />
<strong>aquaculture</strong> <strong>in</strong> coastal areas throughout the world has raised <strong>in</strong>creas<strong>in</strong>g concerns<br />
on its environmental impact (Wu, 1995; Mazzola et al., 1999). Organic and<br />
<strong>in</strong>organic <strong>in</strong>puts have led to a substantial <strong>in</strong>crease of <strong>nutrient</strong> load<strong>in</strong>g <strong>in</strong> coastal<br />
waters.<br />
In general, shrimp culture produces a large amount of waste, <strong>in</strong>clud<strong>in</strong>g nitrogen<br />
and phosphorus, that is released to the aquatic environment. Feed and fertilizer<br />
which are applied <strong>in</strong> shrimp ponds are not fully <strong>in</strong>corporated <strong>in</strong>to the shrimp, but<br />
partly deposited <strong>in</strong> pond sediments or discharged as effluents. In average, shrimp<br />
assimilates only 23-31% of nitrogen and 10-13% of phosphorus of the total<br />
<strong>in</strong>puts. While rema<strong>in</strong><strong>in</strong>g 14-53% of nitrogen <strong>in</strong>puts and 39-67% of phosphorus<br />
<strong>in</strong>puts are deposited <strong>in</strong> the sediment (Dhirendra and L<strong>in</strong>, 2002). Nutrient <strong>in</strong><br />
<strong>aquaculture</strong> effluents are distributed <strong>in</strong> a particulate or soluble fraction (Ackefors<br />
and Enell, 1994). In fresh manure, about 7-32% of total nitrogen (TN) and 30-<br />
84% of total phosphorus (TP) are bound <strong>in</strong> this particulate fraction and the<br />
rema<strong>in</strong>der are excreted <strong>in</strong> dissolved forms (Bergheim et al., 1993). In <strong>in</strong>tensive<br />
mar<strong>in</strong>e shrimp culture, only 24% and 13% of dietary nitrogen and phosphorus<br />
were <strong>in</strong>corporated <strong>in</strong>to harvested shrimp, while the rema<strong>in</strong><strong>in</strong>g <strong>nutrient</strong>s were<br />
released <strong>in</strong>to the surround<strong>in</strong>g water (Briggs and Funge-Smith, 1994). Phosphorus<br />
releases were estimated to be 9.4 kg (Ackefors and Enell, 1990) and 19.6–22.4 kg<br />
(Holby and Hall, 1991) per tonne of shrimp produced.<br />
The <strong>nutrient</strong> releases dur<strong>in</strong>g pond dra<strong>in</strong><strong>in</strong>g at harvest were exceed<strong>in</strong>g or equal<strong>in</strong>g<br />
the limitations recommended by the U.S. Environment Protection Agency (Choo<br />
and Tanaka, 2000). On the other hand, tidal mangrove estuaries impacted by<br />
shrimp pond effluent, have some capacity to process <strong>in</strong>termittent <strong>in</strong>puts of pondderived<br />
<strong>nutrient</strong>s. Mangrove vegetation is capable of remov<strong>in</strong>g excessive<br />
22
<strong>nutrient</strong>s, of up to 70% of <strong>nutrient</strong> <strong>in</strong>put for NO3 - -N and NH4 + -N, reduc<strong>in</strong>g PO4 2- -<br />
P fluctuation, and produc<strong>in</strong>g bioactive compounds (Primavera, 2000).<br />
In recent years, there has been <strong>in</strong>creas<strong>in</strong>g emphasis on develop<strong>in</strong>g treatment<br />
<strong>systems</strong> for aquacultural effluents. Schulz et al. (2003) reported the total<br />
suspended solids (TSS) were reduced by 95.8-97.3% from ra<strong>in</strong>bow trout farm<br />
effluent <strong>in</strong> constructed wetland with emergent plants and subsurface horizontal<br />
water flow. This <strong>nutrient</strong> <strong>in</strong>corporation of co-cultured organisms of different<br />
trophic levels is the basis of environmentally sounded <strong>aquaculture</strong> (Chop<strong>in</strong> et al.,<br />
2001; Neori et al., 2004). Ideally, <strong>nutrient</strong> process <strong>in</strong> polyculture system with two<br />
or more ecologically compatible species should be balanced, waste from one<br />
species are recycled as fertilizer or feed by another without conflict<strong>in</strong>g with each<br />
other (Neori et al., 2000). By <strong>in</strong>tegrat<strong>in</strong>g fed mariculture (fish and shrimp) with<br />
extractive mariculture (seaweed), the wastes of one resource consumer become a<br />
source (fertilizer or feed) for others <strong>in</strong> the system. Such a balanced ecosystem<br />
approach provides <strong>nutrient</strong> bioremediation capacity, mutual benefits to cocultured<br />
organisms, and economic diversification by produc<strong>in</strong>g other value added<br />
materials (Chop<strong>in</strong> et al., 2001).<br />
Silvofisheries or aquasilviculture, <strong>in</strong> which low-density cultures are <strong>in</strong>tegrated <strong>in</strong><br />
mangrove areas, have been reviewed by Primavera (2000). Mangrove ecosystem<br />
plays an obvious role <strong>in</strong> ma<strong>in</strong>ta<strong>in</strong><strong>in</strong>g the biological balance <strong>in</strong> the coastal<br />
environment where shrimp ponds are usually constructed. The removal of<br />
mangroves around shrimp ponds has frequently resulted <strong>in</strong> harvest failure. Boyd<br />
(1999) claimed that mangrove forests are not a suitable site for shrimp farms due<br />
to many reasons such as <strong>in</strong>adequate slope for dra<strong>in</strong>age, excessive organic matter<br />
releases, nitrogen, phosphorus, acid sulphate soil or pyrite discharge. Effluent<br />
treatment <strong>in</strong> shrimp <strong>aquaculture</strong> by macroalgae co-cultivation is still not generally<br />
practiced. However, studies <strong>in</strong>vestigat<strong>in</strong>g the performance of <strong>in</strong>tegrated<br />
mariculture (polyculture) <strong>in</strong> open-waters, have been hampered by the difficulties<br />
<strong>in</strong>volved with the experimental setup and data collection at sea (Petrell and Alie,<br />
1996; Troell et al., 1997; Neori, 2004).<br />
23
In this research, we aim to compare <strong>nutrient</strong> <strong>fluxes</strong> <strong>in</strong> shrimp monoculture with<br />
shrimps and seaweed polyculture <strong>systems</strong> designed to enhance <strong>nutrient</strong> utilization<br />
and to decrease environmental impact of <strong>aquaculture</strong> activities.<br />
Materials and methods<br />
This study was conducted at the Sungai Buntu research station, Research <strong>Institut</strong>e<br />
for Brackish water fisheries, West Java, Indonesia (Figure 1). Shrimp <strong>aquaculture</strong><br />
was <strong>in</strong>tensively carried out for about 3 months from 26 September 2009 to 05<br />
Januar 2010. The experimental site was divided <strong>in</strong>to 3 divisions: Water <strong>in</strong>put<br />
(canal) approximately 1 ha, triplicate of shrimp <strong>aquaculture</strong> ponds (<strong>in</strong>tensive<br />
monoculture) and triplicate of shrimp + seaweed Gracillaria ponds (<strong>in</strong>tensive<br />
polyculture) (Figure 2). The area of each pond was 1200 m 2 (40 m x 30 m) and<br />
the water depth of each pond was 1 m.<br />
Location of experiments<br />
(Sungai Buntu-West Java)<br />
Figure 1. Map of Research <strong>Institut</strong>e for Brackish water fisheries, West Java,<br />
Indonesia<br />
24
Ocean<br />
(North<br />
Java Sea)<br />
Fresh Fresh sea Water<br />
water <strong>in</strong>put A <strong>in</strong>put<br />
Chanel<br />
Water Stock<br />
B B B<br />
C C C<br />
River<br />
Intensive monocilture<br />
system<br />
Waste Waste water water output<br />
output<br />
Intensive polyculture<br />
system<br />
Sampl<strong>in</strong>g po<strong>in</strong>t:<br />
A. Water <strong>in</strong>flow<br />
B. Polyculture system<br />
C. Monoculture system<br />
: Gracilaria<br />
Figure 2. Schematic outl<strong>in</strong>e of shrimp monoculture and polyculture <strong>systems</strong><br />
Each pond was fertilized with 3 kg of urea before stock<strong>in</strong>g of shrimp and<br />
Gracillaria. Fertilizers were used to <strong>in</strong>crease primary productivity or natural food<br />
establishment <strong>in</strong> ponds.<br />
The seaweed Gracillaria (Gracillaria verrucosa), provided from local production<br />
<strong>in</strong> Sungai Buntu, Karawang-West Java was <strong>in</strong>serted <strong>in</strong>to polyethylene ropes that<br />
were fixed by the rafts. A suspension culture unit was composed of four rafts,<br />
each <strong>in</strong> turn of n<strong>in</strong>e ropes. Each rope (about 10 m long) was <strong>in</strong>serted with a piece<br />
of alga (15 g) every 20 cm. Distance between adjacent ropes was 50 cm and<br />
between adjacent units distance was 3 m.<br />
Shrimp Penaeus vannamei post larvae (0.22 ± 0.016 g/<strong>in</strong>d) were stocked at a<br />
density of 20 <strong>in</strong>dividuals/m 2 (Table 2) <strong>in</strong> each of the 6 ponds. Triplicate<br />
polyculture ponds of 1200 m² were additionally stocked with Gracillaria. Before<br />
stock<strong>in</strong>g, shrimp were acclimatized for one night to the pond water conditions.<br />
Control sampl<strong>in</strong>g of shrimp weight ga<strong>in</strong> was realized every 10 days to determ<strong>in</strong>e<br />
the actual weight for feed application. 5 <strong>in</strong>dividuals were taken to be weighed.<br />
Feed supplied equaled to 7-10% of shrimp biomass <strong>in</strong> accordance to time after<br />
control sampl<strong>in</strong>g (modified after Baliao and Tookw<strong>in</strong>as, 2002). At day 0 and day<br />
1 after sampl<strong>in</strong>g, daily feed supply amounted 7%, from day 2 until day 4 8%,<br />
from day 5 until day 7 9% and from day 8 until day 9 10%. Feed was given 4<br />
25
times a day, i.e. at 07.00, 12.00, 17.00 and 22.00. Two percent of the water<br />
volume of the shrimp ponds was added every day.<br />
Every 10 days ponds were monitored to estimate the survival rate (SR) of shrimp.<br />
Survival rate (SR) was calculated as ratio between the numbers of shrimp at a<br />
certa<strong>in</strong> time (at sampl<strong>in</strong>g) to the number of shrimp at the time of stock<strong>in</strong>g. To<br />
determ<strong>in</strong>e the number of shrimp at sampl<strong>in</strong>g follow<strong>in</strong>g formula were used:<br />
Nt = Nu * Lt / Lj<br />
Description:<br />
Nt = number of shrimp <strong>in</strong> ponds at time-t<br />
Nu = number of shrimp caught <strong>in</strong> nets at each sampl<strong>in</strong>g time-t<br />
Lt = pond area (m 2 )<br />
Lj = net effective aperture area (m 2 ).<br />
Nutrient sampl<strong>in</strong>g<br />
Every 10 days, the water quality (ammonium-nitrogen, nitrate-nitrogen, nitritenitrogen,<br />
orthophosphate-phosphorus and hydrogen sulphide) were analysed. The<br />
samples were taken over 24 hours by <strong>in</strong>tervals of 3 hours. Water sample were<br />
taken 20 cm below the water surface. Every day at 08.00 and 16.00, water<br />
temperature, sal<strong>in</strong>ity, and dissolved oxygen (DO) were monitored <strong>in</strong> situ with a<br />
portable water quality sensor system (TOA model WQC-20A electronic Ltd.,<br />
Japan). Water samples were collected us<strong>in</strong>g plastic bottles <strong>in</strong>stalled at the edge of<br />
a stick. They were immediately filtered through Whatman GF/F filters 0.7 µM<br />
millipore for soluble <strong>nutrient</strong>s analyses (PO4 -3 , NO3 - , NO2 _ , NH4 + ). The<br />
ammonium-nitrogen concentration <strong>in</strong> the filtrate was measured immediately after<br />
filtration. Total nitrogen (TN), total phosphorus (TP), nitrate-nitrogen, nitritenitrogen,<br />
and orthophosphat concentrations were measured by the APHA (1995)<br />
standard method. The <strong>nutrient</strong> analyses were performed by spectrophotometer<br />
(Shimadzu UV-2400).<br />
The standard methods for the determ<strong>in</strong>ation of ammonium-, nitrite- and nitratenitrogen<br />
were based on moderate alkal<strong>in</strong>e solution with hypochlorite,<br />
diazotization and cadmium reduction followed by diazotization, respectively. The<br />
standard method for the determ<strong>in</strong>ation of orthophosphat was based on the reaction<br />
26
of the phosphorus ions with an acidified molybdate reagent. The<br />
spectrophotometer wave length for ammonium-nitrogen, nitrite-nitrogen, nitratenitrogen<br />
and phosphorus were 630 nm, 542 nm, 542 nm and 882 nm, respectively.<br />
Pre-ashed (500 °C) and weight of GF/F filters <strong>in</strong> glass dishes were used to<br />
determ<strong>in</strong>e suspended solids <strong>in</strong> accordance to standard filtration method<br />
(APHA,1995). Nitrogen and phosporus content <strong>in</strong> organic matter of shrimp feed,<br />
shrimp, Gracillaria and total suspended solids were measured us<strong>in</strong>g Kjehdahl<br />
method. H2S was measured by Cl<strong>in</strong>e methode based on N, N-dimethyl-pphenylenediam<strong>in</strong>e<br />
(Cl<strong>in</strong>e, 1968).<br />
Statistics<br />
Water quality and <strong>nutrient</strong> <strong>fluxes</strong> from water <strong>in</strong>flow, monoculture and polyculture<br />
ponds were analyzed statistically. All data were checked for normality<br />
(Kolmogorov – Smirnov test) and homogeneity of variances (HOV, Brown<br />
Forsythe test). Differences of means of triplicate ponds (n=3) were evaluated for<br />
significance by the range tests of Tukey HSD (P
Result and discussion<br />
Water quality<br />
Water temperature ranged from 23.7–28.7 ºC. Average values of temperature<br />
ranged between 26.5–27.8 o C at sampl<strong>in</strong>g po<strong>in</strong>ts. Sal<strong>in</strong>ity also showed no<br />
significant difference between the mono- and polyculture <strong>systems</strong> (P>0.05).<br />
Average values of sal<strong>in</strong>ity for <strong>in</strong>flow water (canal), monoculture and polyculture<br />
ponds were 36.7 ppt, 38.2 ppt and 37.7 ppt, respectively (Table 1). This values<br />
were high as the experiments were realized dur<strong>in</strong>g dry season. Dissolved oxygen<br />
<strong>in</strong> water is the most important factor which determ<strong>in</strong>es water quality for<br />
aquacultural purposes. Appropriate dissolved oxygen (DO) level for shrimp<br />
<strong>aquaculture</strong> are higher than 3 mg/l. In this study, the average of dissolved oxygen<br />
(DO) over 100 days period <strong>in</strong> monoculture was 3.03 mg/l while <strong>in</strong> polyculture<br />
significantly higher DO values of 4.77 mg/l were recorded (Tabel 1). It can be<br />
assumed that <strong>in</strong> day light, Gracillaria produces sufficient amounts of oxygen by<br />
photosynthesis activities.<br />
Table 1. Water quality parameter over 100 days period<br />
Parameter Inflow Monoculture Polyculture<br />
Temperature ( o C) 27.84 a 26.5±1.02 a 26.50±1.05 a<br />
Dissolved oxygen (mg/l) 4.2 a 3.03±0.58 b 4.77±0.67 a<br />
Sal<strong>in</strong>ity (ppt) 36.7 a 38.18±0.74 a 37.72±0.57 a<br />
pH 7.75 a 7.77±0.15 a 7.73±0.17 a<br />
TSS (mg/l)* 15.6 a 59.89±8.44 b 56.5±7.53 b<br />
TN (mg/l)* 0.95 a 2.97±0.50 b 3.2±0.33 b<br />
TP (mg/l)* 0.17 a 1.3±0.19 b 1.1±0.22 b<br />
NH4 + -N (mg/l) 0.014 a 0.37±0.04 b 0.24±0.03 c<br />
NO3 - -N (mg/l) 0.004 a 0.018±0.001 b 0.017±0.001 b<br />
NO2 - -N (mg/l) 0.0002 a 0.002±0.0005 b 0.002±0.0004 b<br />
PO4-P (mg/l) 0.001 a 0.005±0.0006 b 0.004±0.0008 b<br />
Values given are means of 10 times sampl<strong>in</strong>g <strong>in</strong> triplicate ponds. (*TSS, TN, and TP are<br />
means of 4 times sampl<strong>in</strong>g <strong>in</strong> triplicate ponds).<br />
Values with the same superscript letter do not differ significantly (P>0.05).<br />
28
Xu (2008) reported the Gracillaria cultivation can improve other aspects of water<br />
quality <strong>in</strong>stead of <strong>in</strong>creas<strong>in</strong>g DO. Its photosynthesis produces DO that promotes<br />
decomposition of organics. Density raft culture of Gracillaria impedes the water<br />
circulation and may decrease chemical oxygen demand (COD) <strong>in</strong> the water<br />
column. In addition, several species of Gracillaria can produce oxygen under low<br />
light condition, such as <strong>in</strong> ra<strong>in</strong>y days and remediate anoxia (Xu et al., 2004).<br />
Concentration (m g/l)<br />
0.02<br />
0.018<br />
0.016<br />
0.014<br />
0.012<br />
0.01<br />
0.008<br />
0.006<br />
0.004<br />
0.002<br />
0<br />
0 20 40 60 80 100 120<br />
a<br />
b<br />
c<br />
Time (days)<br />
a<br />
c<br />
a<br />
a<br />
a<br />
c<br />
a<br />
c<br />
b<br />
Polyculture<br />
Monoculture<br />
Inflow<br />
Figure 3. Concentration of H2S dur<strong>in</strong>g the experimental period, values are<br />
mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05).<br />
Hydrogen sulfide (H2S) can severely affect shrimp growth <strong>in</strong> pond. H2S is<br />
produced by chemical reduction of organic matter that accumulates and forms a<br />
thick layer of organic deposits at the bottom. High levels of hydrogen sulfide<br />
would affect directly demersal or burrow<strong>in</strong>g shrimps such as Peneaus monodon.<br />
At levels of 0.1–0.2 mg/l of H2S <strong>in</strong> the water, shrimp growth will be disturbed and<br />
die <strong>in</strong>stantly at concentration higher than 4 mg/l (Law, 1988). In this study,<br />
hydrogen sulfide (H2S) presented after 60 days. Highest hydrogen sulfide (H2S)<br />
levels of 0.018 mg/l were recorded at harvest for the monoculture system and of<br />
29
0.009 mg/l for the polyculture system (figure 3). This means that H2S was not<br />
harmful for the growth of shrimp <strong>in</strong> monoculture and polyculture system.<br />
Nutrients <strong>fluxes</strong><br />
Dissolved <strong>nutrient</strong> fixation is one of the core advantages of constructed wetlands<br />
compared to standard mechanical effluent treatment (Schulz, 2003). In this study,<br />
the ammonium concentration <strong>in</strong>creased gradually <strong>in</strong> monoculture and polyculture<br />
<strong>systems</strong> and orthophosphate concentration progressively <strong>in</strong>creased as well.<br />
Though well water was supplied to the pond, the ammonium-nitrogen<br />
concentrations <strong>in</strong> monoculture <strong>in</strong>creased from 0.005 to 0.779 mg/l (Figure 4), with<br />
an average concentration of ammonium-nitrogen dur<strong>in</strong>g the 100 days period of<br />
0.37 mg/l (Table 1). In polyculture system, it <strong>in</strong>creased from 0.003 to 0.483 mg/l<br />
(Figure 4), with an average of 0.24 mg/l. Therefore, ammonium-nitrogen<br />
concentrations were significantly higher <strong>in</strong> comparison to polyculture system<br />
(P0.05).<br />
30<br />
Monoculture<br />
Polyculture<br />
Inflow
Concentration (mg/l)<br />
Concentration (mg/l)<br />
0.045<br />
0.04<br />
0.035<br />
0.03<br />
0.025<br />
0.02<br />
0.015<br />
0.01<br />
0.005<br />
0<br />
a<br />
a<br />
a<br />
a<br />
a<br />
b<br />
a b b<br />
a<br />
a<br />
a<br />
a<br />
a<br />
b b b<br />
a<br />
0 20 40 60 80 100 120<br />
b<br />
a<br />
a<br />
Time (days)<br />
Figure 5. Concentrations of nitrate-nitrogen (NO3 + -N) dur<strong>in</strong>g the<br />
experimental period, values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05).<br />
0.008<br />
0.007<br />
0.006<br />
0.005<br />
0.004<br />
0.003<br />
0.002<br />
0.001<br />
0<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a a<br />
a a a<br />
a a<br />
a<br />
a<br />
b<br />
b b b b b b<br />
a a<br />
a<br />
a<br />
a<br />
0 20 40 60 80 100 120<br />
Time (days)<br />
Figure 6. Concentrations of nitrite-nitrogen (NO2 + -N) dur<strong>in</strong>g the<br />
experimental period, values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05).<br />
a<br />
b<br />
a<br />
a<br />
b<br />
a<br />
a<br />
a<br />
b<br />
Monoculture<br />
Polyculture<br />
Inflow<br />
Monoculture<br />
polyculture<br />
Inflow<br />
Low values of nitrate- and nitrite-nitrogen, of 0.0044 and 0.0002 mg/l (Table 1)<br />
were observed <strong>in</strong> the pond <strong>in</strong>let and higher values were generated, possibly by<br />
nitrification bacteria <strong>in</strong> the pond <strong>systems</strong>. Nevertheless, no differences could be<br />
31
observed for nitrate and nitrite <strong>in</strong> monoculture or polyculture <strong>systems</strong> dur<strong>in</strong>g the<br />
experiment (P>0.05) (Figures 5 and 6). The average concentration of nitrate and<br />
nitrite-nitrogen <strong>in</strong> the monoculture system were 0.018 and 0.002 mg/l,<br />
respectively, and 0.017 and 0.002 mg/l <strong>in</strong> polyculture system (Table 1).<br />
Hopk<strong>in</strong>s et al. (1995) found that particulate matter and dissolved <strong>nutrient</strong>s <strong>in</strong> the<br />
outflow water <strong>in</strong>creased considerably with higher water exchange rates. The<br />
authors concluded that assimilation by phytoplankton and nitrify<strong>in</strong>g bacteria<br />
attached to detritus particles are the ma<strong>in</strong> processes of nitrogen removal from the<br />
water column Hargreaves (1998) suggests that the potential for N removal from<br />
ponds by denitrification is high.<br />
Concentration (mg/l)<br />
9<br />
8<br />
7<br />
6<br />
5<br />
4<br />
3<br />
2<br />
1<br />
0<br />
a a<br />
b<br />
a<br />
b<br />
0 20 40 60 80 100 120<br />
a<br />
Time (days)<br />
a<br />
b<br />
a<br />
Polyculture<br />
Monoculture<br />
Inflow<br />
Figure 7. Concentrations of Total Nitrogen (TN) dur<strong>in</strong>g the experimental<br />
period, values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05).<br />
32
concentration (mg/l)<br />
0.01<br />
0.008<br />
0.006<br />
0.004<br />
0.002<br />
0<br />
a<br />
a<br />
b<br />
a<br />
b<br />
a a a a<br />
b<br />
b b<br />
a<br />
b<br />
a<br />
a<br />
b b<br />
0 20 40 60 80 100 120<br />
a<br />
Time (days)<br />
a<br />
a a<br />
a<br />
a a a<br />
b<br />
b b b<br />
Monoculture<br />
Polyculture<br />
Inflow<br />
Figure 8. Concentration of Orthophosphate (PO4) dur<strong>in</strong>g the experimental<br />
period, values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05).<br />
Concentration (mg/l)<br />
3.5<br />
3<br />
a<br />
2.5<br />
2<br />
a<br />
a<br />
1.5<br />
a<br />
1<br />
0.5<br />
0<br />
b<br />
a<br />
a<br />
b<br />
b<br />
-0.5 0 20 40 60<br />
Time (days)<br />
80 100 120<br />
Polyculture<br />
Monoculture<br />
Inflow<br />
Figure 9. Concentrations of Total Phosphorus (TP) dur<strong>in</strong>g the experimental<br />
period, values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05).<br />
33
Total nitrogen (TN) and total phosphorus (TP) concentration <strong>in</strong>creased <strong>in</strong> the<br />
outlet water of polyculture and monoculture ponds. TN <strong>in</strong> polyculture ponds<br />
<strong>in</strong>creased from 0.15-7.43 mg/l (Figure 7), with an average of 3.2 mg/l (Table 1),<br />
while <strong>in</strong> monoculture TN ranged from 0.13–7.26 mg/l (Figure 7), with an average<br />
of 2.97 mg/l (Table 1). TP <strong>in</strong> polyculture pond <strong>in</strong>creased from 0.015–2.83 mg/l<br />
(Figure 9), with an average of 1.1 mg/l (Table 1), while <strong>in</strong> monoculture values of<br />
0.013–2.41 mg/l (Figure 9) and an average of 1.3 mg/l (Table 1) could be<br />
observed, but no significant differences (P>0.05) could be observed between the<br />
<strong>systems</strong>.<br />
The average concentrations of orthophosphate <strong>in</strong> the <strong>in</strong>let water, monoculture and<br />
polyculture effluents dur<strong>in</strong>g the 100 days period were 0.001, 0.005 and 0.004<br />
mg/l, respectively (Table 1). There were no significant differences between<br />
monoculture and polyculture system (P>0.05). Orthophosphate <strong>in</strong>creased from<br />
0.0012 mg/l to 0.0081 mg/l for monoculture and 0.0012 mg/l to 0.0067 mg/l for<br />
the polyculture <strong>systems</strong> (Figure 8). It can be assumed that the <strong>in</strong>itial concentration<br />
of phosphorus was not <strong>in</strong>fluenced by <strong>in</strong>flow<strong>in</strong>g phosphorus.<br />
34
Table 2. Performance of experimental <strong>in</strong>tensive shrimp polyculture and<br />
monoculture system over 100 days period (n=3)<br />
Parameter Polyculture Monoculture<br />
Stocked larvae:<br />
Stock<strong>in</strong>g density<br />
(Individuals/m 2 )<br />
Total larvae (<strong>in</strong>d)<br />
Weight (g/<strong>in</strong>d)<br />
Total weight (kg)<br />
20<br />
24000<br />
0.22 ± 0.016<br />
5.1<br />
20<br />
24000<br />
0.22 ± 0.016<br />
5.1<br />
Culture time (days) 100 100<br />
At harvest:<br />
Shrimp (<strong>in</strong>d/ m 2 )<br />
Total shrimp<br />
Individual weight<br />
(g/<strong>in</strong>d)<br />
Weight (kg/m 2 )<br />
Total weight (kg)<br />
16.8 a<br />
20141 a<br />
24.9 ± 1.8 a<br />
0.42<br />
501.5<br />
13.5 b<br />
16140 b<br />
20.8 ± 1.05 b<br />
0.28<br />
335.7<br />
Survival rate (%) 86.32 a 69.17 b<br />
Total Feed (kg) 826.7 a 620 b<br />
FCR 1.67 a 1.88 b<br />
Values with the same superscript letter do not differ significantly (P>0.05).<br />
Seventy thousand post larvae (PL) were stocked <strong>in</strong> the triplicate ponds with a<br />
density of 20 <strong>in</strong>d/m 2 . Initial weight of <strong>in</strong>dividual larvae (PL) was 0.22 ± 0.016 g<br />
result<strong>in</strong>g <strong>in</strong> a total stock<strong>in</strong>g weight of approximately 5.1 kg/1200 m 2 .<br />
Approximately 826.7 kg/ of pelleted feed was supplied for each polyculture<br />
system pond and 620 kg for the triplicate monoculture ponds (Table 2). 501.5<br />
kg/1200 m 2 of shrimp were harvested for the polyculture system and 335.7<br />
kg/1200 m 2 for the monoculture system (Table 2). Feed given to the polyculture<br />
ponds was higher compared to the monoculture shrimp due to the higher growth<br />
performance <strong>in</strong> polyculture ponds. The average f<strong>in</strong>al weight of shrimp was 24.9 ±<br />
35
1.8 g for polyculture <strong>systems</strong> with survival rates of 86.3%. For monoculture, the<br />
weight of shrimp was 20.8 ± 1.05 g and survival rate accounted 69.17% (Table 2).<br />
Survival rate of shrimp <strong>in</strong> polyculture was significantly higher than <strong>in</strong><br />
monoculture, and the weight of shrimp as well (P
Mass balance<br />
Mass Balance calculations for <strong>nutrient</strong>s are important to evaluate the efficiency of<br />
feed <strong>nutrient</strong> utilization <strong>in</strong> order to estimate the pollut<strong>in</strong>g potential of pond<br />
effluents (Tucker and Boyd, 1985; Briggs and Simon, 1994).<br />
TN-mass balance polyculture system<br />
Fertilization<br />
3% (1.56 kg)<br />
Water <strong>in</strong>flow<br />
6.9%<br />
(3.65 kg)<br />
Seaweed stocked<br />
0.04%<br />
(0.02 kg)<br />
Stocked shrimp<br />
0.06%<br />
(0.03 kg)<br />
Shrimp feed 90%<br />
(47.6 kg) a<br />
Shrimp feed 90%<br />
(47.6 kg) a<br />
TN-mass balance monoculture system<br />
Fertilization<br />
3.8% (1.56 kg)<br />
Water <strong>in</strong>flow<br />
8.9% (3.65 kg)<br />
Shrimp stocked<br />
TP-mass balance polyculture system<br />
Seaweed Stocked<br />
0.06%<br />
(0.006 kg)<br />
Shrimp stocked<br />
0.2%<br />
(0.02 kg)<br />
Fertilization<br />
2% (0.2 kg)<br />
Water <strong>in</strong>flow<br />
6.2% (0.6)<br />
TP-mass balance monoculture system<br />
Fertilization<br />
2.7% (0.2 kg)<br />
Water <strong>in</strong>flow<br />
7.9% (0.6 kg)<br />
Shrimp stocked<br />
0.3%<br />
(0.02 kg)<br />
Shrimp food<br />
91.74% (8.9 kg) a<br />
Shrimp harvest<br />
6.9% (0.67 kg) a<br />
Shrimp food<br />
91.74% (8.9 kg) a<br />
Shrimp harvest<br />
6.9% (0.67 kg) a<br />
Shrimp food<br />
89.1% (6.7 kg) b<br />
Shrimp food<br />
89.1% (6.7 kg) b<br />
Seaweed<br />
harvest 2.4%<br />
(0.23 kg)<br />
Pond Water<br />
Shrimp harvest<br />
5.3% (0.4 kg) b<br />
Shrimp harvest<br />
5.3% (0.4 kg) b<br />
Pond Water<br />
Others<br />
Associated<br />
43.4%<br />
(4.23 kg)<br />
Outlet<br />
water<br />
47.3%<br />
(4.6 kg) a<br />
Outlet<br />
water<br />
47.3%<br />
(4.6 kg) a<br />
Others<br />
Associated<br />
42.8%<br />
(3.22 kg)<br />
Outlet<br />
water<br />
51.9%<br />
(3.9 kg) a<br />
Outlet<br />
water<br />
51.9%<br />
(3.9 kg) a<br />
Figure 11. Total phosphate mass balance <strong>in</strong> experimental polyculture and<br />
monoculture <strong>systems</strong>. Values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly between mono- and<br />
polyculture <strong>systems</strong> (P>0.05).<br />
38
Us<strong>in</strong>g the strategy proposed by Funge-Smith and Briggs (1998), a mass balance<br />
for the fate of <strong>nutrient</strong>s <strong>in</strong> feed added to shrimp ponds was developed based on the<br />
<strong>nutrient</strong> amount of feed and fertilizer added, shrimp and Gracillaria stocked,<br />
shrimp and Gracillaria harvested, and <strong>nutrient</strong>s <strong>in</strong> and out-flow<strong>in</strong>g water.<br />
Each pond was fertilized with approximately 3 kg urea/1200 m 2 before stock<strong>in</strong>g.<br />
Total nitrogen (TN) and total phosphate (TP) from fertilizer were 1.56 kg/1200 m 2<br />
and 0.2 kg/1200 m 2 for the monoculture and polyculture system. Whereas TN and<br />
TP from <strong>in</strong>flow<strong>in</strong>g water were 3.65 kg/1200 m 2 and 0.6 kg/1200 m 2 for the<br />
monoculture and polyculture system (Figures 10 and 11). Outlet water conta<strong>in</strong>ed<br />
10.4 kg/1200 m 2 and 3.9 kg/1200 m 2 of total nitrogen (TN) and total phosphorus<br />
(TP), for the monoculture system and 11.27 kg/1200 m 2 and 4.6 kg for the<br />
polyculture system (Figures 10 and 11).<br />
Figure 10 and 11 showed total nitrogen and total phosphorus mass balance <strong>in</strong><br />
polyculture system with a growth performance of 0.42 kg shrimp m -2 and 0.3 kg<br />
Gracillaria m -2 and a feed conversion ratio of 1.67 (shrimp: 34.5% dry matter,<br />
9.4% N, 0.38% P; Feed: 90% dry matter) and with 0.28 kg shrimp m -2 and a feed<br />
conversion ratio of 1.88 (shrimp: 33% dry matter, 8.9% N, 0.3% P; Feed: 90% dry<br />
matter) <strong>in</strong> monoculture system.<br />
In addition, monoculture system were characterised by 8.9% and 0.3% of applied<br />
total nitrogen (TN) and total phosphorus (TP) <strong>in</strong>corporated <strong>in</strong> shrimp and 9.4%<br />
and 0.38% <strong>in</strong> shrimps of the polyculture system. Gracillaria <strong>in</strong>corporated 3.31%<br />
and 0.42% of total nitrogen (TN) and total phosphorus (TP) <strong>in</strong> polyculture<br />
system. When shrimp were harvested, at least about 24.2% of the total nitrogen<br />
(TN) and 5.3% of the total phosphorus (TP) for the monoculture system and about<br />
34.3% (30.8% from shrimp harvest and 3.5% from seaweed harvest) of the total<br />
nitrogen (TN) and 9.3% (6.9% from shrimp harvest and 2.4% from seaweed<br />
harvest) of the total phosphorus (TP) for the polyculture system were removed<br />
(Figures 10 and 11). Total nitrogen and total phosphorus <strong>in</strong> outlet water amounted<br />
10.4 kg/1200 m 2 and 3.9 kg/1200 m 2 <strong>in</strong> the monoculture system. In the<br />
polyculture ponds 11.27 kg/1200 m 2 and 4.6 kg/1200 m 2 of TP and TN were<br />
recorded <strong>in</strong> outlet water (Figures 10 and 11).<br />
39
The largest source of nitrogen orig<strong>in</strong>ated from feed with 87.2% for the<br />
monoculture and 90% for the polyculture system. The rema<strong>in</strong><strong>in</strong>g nitrogen derived<br />
from fertilizer and <strong>in</strong>flow<strong>in</strong>g water, 3.8% and 8.9% for the monoculture and 3%<br />
and 6.9% for the polyculture system (Figure 10). Outlet water conta<strong>in</strong>ed 25.4% of<br />
total nitrogen for the monoculture and 21.3% for the polyculture system (Figure<br />
10). Denitrification, ammonium volatilization and total nitrogen <strong>in</strong> other organism<br />
e.g. benthos and zooplankton were not directly evaluated <strong>in</strong> this study, but 50.4%<br />
of total nitrogen <strong>in</strong>put for the monoculture and 44.4% for the polyculture system<br />
could be analyzed as unidentified losses. This loss of nitrogen was assumed to be<br />
lost to the atmosphere as N2 via denitrification. The volatilization of nitrogen<br />
emphasizes the significance of microbial decomposition process <strong>in</strong> ponds.<br />
Another possibility for this loss of nitrogen could be the <strong>in</strong>corporation <strong>in</strong>to other<br />
organisms. Hopk<strong>in</strong>s et al. (1993) could not account for 13 - 46% of total nitrogen<br />
<strong>in</strong>put <strong>in</strong> <strong>in</strong>tensive shrimp ponds. 27.4% of the total nitrogen was unaccounted <strong>in</strong> a<br />
semi <strong>in</strong>tensive shrimp farm <strong>in</strong> North-Western Mexico expla<strong>in</strong>ed by denitrification<br />
and atmospheric diffusion of unionized ammonia (Paez-Osuna et al. 1997).<br />
N-fixation by blue-green algae was not taken <strong>in</strong>to account by the model, and the<br />
significance of this contribution is unknown. In this model, the amount of nitrogen<br />
from stock<strong>in</strong>g larvae and Gracillaria were only 0.03 kg/1200 m 2 and 0.02<br />
kg/1200 m 2 respectively.<br />
The nitrogen mass balance reveal <strong>in</strong> detail, the source and s<strong>in</strong>k of the organic<br />
component <strong>in</strong> a shrimp pond. Funge-Smith and Briggs (1998) reported the actual<br />
amount of <strong>nutrient</strong>s assimilated <strong>in</strong>to shrimp biomass is a small fraction of the total<br />
amount applied as feed. Only 18-27% of nitrogen applied to the pond was<br />
assimilated <strong>in</strong>to shrimp, thus there is considerable wastage as <strong>nutrient</strong>s are<br />
<strong>in</strong>corporated <strong>in</strong>to plankton biomass, volatilized or trapped <strong>in</strong> the sediment. The<br />
s<strong>in</strong>ks for nitrogen are the sediments (24%), harvested shrimp (18-27%) and<br />
discharge water (27%). Approximately 30% of the nitrogen unaccounted is<br />
assumed to be N losses to the atmosphere as N2 or ammonia.<br />
The largest source of total phosphorus (TP) orig<strong>in</strong>ated from feed, 89.1 % for the<br />
monoculture and 91.74% for the polyculture system. The rest of TP derived from<br />
fertilizer and water <strong>in</strong>put were 2.7% and 7.9% for the monoculture <strong>systems</strong> and<br />
40
2% and 6.2% for the polyculture system, respectively (Figure 11). Total<br />
phosphorus <strong>in</strong> outlet water was 51.9% <strong>in</strong> the monoculture and 47.3% <strong>in</strong> the<br />
polyculture system of total phosphorus <strong>in</strong>put (Figure 11). That means, 51.9% of<br />
total phosphorus <strong>in</strong>put for monoculture and 47.3% of total phosphorus <strong>in</strong>put for<br />
polyculture system were discharged to the environment. TP associated <strong>in</strong> other<br />
organisms e.g. benthos and zooplankton was not directly evaluated <strong>in</strong> this study,<br />
but 42.8% of total phosphorus <strong>in</strong>put for the monoculture and 43.4% for the<br />
polyculture system were unaccounted. It can be assumed that this amount is lost<br />
through consumption by other macrofauna or fixed <strong>in</strong> m<strong>in</strong>erals <strong>in</strong> sediment.<br />
The processes of denitrification, ammonia volatilization and phosphorus<br />
adsorption by sediments serve to regulate their concentrations <strong>in</strong> the water column<br />
(Tucker and Boyd, 1985). Boyd (1985) reported that 56% of phosphorus <strong>in</strong>puts <strong>in</strong><br />
freshwater catfish ponds was lost through uptake by sediments. Briggs and Funge-<br />
Smith (1994) reported that 84% of the phosphorus was reta<strong>in</strong>ed <strong>in</strong> the sediments<br />
of <strong>in</strong>tensive mar<strong>in</strong>e shrimp ponds <strong>in</strong> Thailand. Funge-Smith and Briggs (1998)<br />
reported the pr<strong>in</strong>cipal source of phosphorus <strong>in</strong> <strong>in</strong>tensive shrimp ponds was the<br />
applied feed (51%). The 26% shortfall <strong>in</strong> <strong>in</strong>puts was assumed to be the eroded<br />
pond bottom. Effluent water constituted 10% of TP loss <strong>in</strong> the budget and this is<br />
ma<strong>in</strong>ly bound <strong>in</strong> the suspended solid fraction. Thus, trapp<strong>in</strong>g of the suspended<br />
solid fraction is important to m<strong>in</strong>imize its environmental impact.<br />
Effluents from shrimp <strong>aquaculture</strong> typically were enriched <strong>in</strong> suspended solid and<br />
<strong>nutrient</strong>s. Different alternatives have been considered to mitigate or resolve the<br />
impact of shrimp pond effluents on the water quality of adjacent coastal waters.<br />
The use of polyculture technology, with shrimp and seaweed, have been<br />
positively evaluated <strong>in</strong> this study. Improved pond design, construction of buffer<br />
ponds, reduction and elim<strong>in</strong>ation of water exchange rates are other <strong>in</strong>terest<strong>in</strong>g<br />
alternatives that could reduce the impact of shrimp pond effluents (Paez-Osuna,<br />
2000), but for marg<strong>in</strong>al areas polyculture seems to be a viable way to <strong>in</strong>crease<br />
<strong>nutrient</strong> efficiencies <strong>in</strong> shrimp <strong>aquaculture</strong>.<br />
41
Conclusions<br />
The seaweed Gracillaria can be cultivated <strong>in</strong> polyculture with shrimp. This<br />
macroalgae can not only serve as an effective biofilter for shrimp ponds but also<br />
can <strong>in</strong>crease shrimp productivity. The weight and survival rate of shrimp <strong>in</strong><br />
polyculture <strong>systems</strong> were higher than <strong>in</strong> monoculture. The <strong>nutrient</strong>s <strong>fluxes</strong><br />
demonstrate a high efficiency <strong>in</strong> polyculture <strong>systems</strong> than <strong>in</strong> monoculture. The<br />
polyculture us<strong>in</strong>g Gracillaria as co-cultivation may thus encourage future<br />
polyculture <strong>systems</strong> to be adopted by farmers as an environmentally friendly way<br />
of <strong>aquaculture</strong>.<br />
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Xu, Y. J., J. Fang, Q. Tang, J. L<strong>in</strong>, G. Le. 2008. Improvement of water quality by<br />
the macroalga, Gracilaria lemaneiformis (Rhodophyta), near <strong>aquaculture</strong><br />
effluent outlets. World Aquaculture Society. 39. 549-555.<br />
45
Chapter 3: Nutrient Fluxes and Mass Balances <strong>in</strong> Various<br />
Polyculture Systems Us<strong>in</strong>g Shrimp (Penaeus vannamei), Fish<br />
(Oreochromis sp.) and Seaweed (Gracillaria verrucosa)<br />
Y. N. Ihsan ab , K. J. Hesse c , C. Schulz ab<br />
a Gesellschaft <strong>für</strong> Mar<strong>in</strong>e Aquakultur mbH, Hafentörn 3, D-25761 Büsum<br />
b <strong>Institut</strong>e for Animal Breed<strong>in</strong>g and Husbandry, Christian-Albrechts-Universität<br />
D-24098 Kiel<br />
c Research and Technology Centre, Christian-Albrechts-Universität<br />
D-25761 Büsum<br />
Submitted to the Journal of World Aquaculture Society<br />
46
Abstract<br />
A comparative study on polyculture <strong>systems</strong> us<strong>in</strong>g various comb<strong>in</strong>ations of<br />
shrimp (Penaeus vannamei), seaweed Gracillaria (Gracillaria verrucosa), and<br />
fish (Oreochromis sp.) was conducted <strong>in</strong> order to calculate <strong>nutrient</strong>s <strong>fluxes</strong> and<br />
mass balances. Therefore, triplicate ponds of 1000 m 2 size were stocked with 0.4<br />
kg/m 2 seaweed and 15 shrimps/m 2 (polyculture I), and triplicate ponds of size<br />
1000 m 2 were stocked with 0.4 kg/m 2 seaweed, 15 shrimps/m 2 , and 0.25 fish/m 2<br />
(polyculture II). Every 10 days dur<strong>in</strong>g the 90-day culture period, pooled 24hwater<br />
samples were taken to describe <strong>nutrient</strong> <strong>fluxes</strong> <strong>in</strong> the ponds. Water quality<br />
<strong>in</strong> both polyculture <strong>systems</strong> were with<strong>in</strong> the physiological ranges for the shrimp,<br />
with whole period average total suspended solids (TSS) concentrations of 50.5 ±<br />
7.6 mg/l <strong>in</strong> polyculture I, while <strong>in</strong> polyculture II TSS was 64.9 ± 4.2 mg/l. The<br />
average total nitrogen (TN) and total phosphorus (TP) amount <strong>in</strong> polyculture I<br />
were 2.25 ± 0.4 mg/l and 0.84 ± 0.05 mg/l, respectively, while <strong>in</strong> polyculture II<br />
TN and TP amounted 2.66 ± 0.8 mg/l and 0.89 ± 0.05 mg/l, respectively. A mass<br />
balance model was developed for total nitrogen and total phosphorus to estimate<br />
their <strong>fluxes</strong>. From total nitrogen and total phosphorus <strong>in</strong>put, 46.79% and 14.99%<br />
were <strong>in</strong>corporated <strong>in</strong> 313.08 kg/1000 m 2 shrimp weight ga<strong>in</strong> <strong>in</strong> polyculture system<br />
I, while 41.47% and 13.47% were <strong>in</strong>corporated <strong>in</strong> 291.25 kg/1000m 2 shrimp<br />
weight ga<strong>in</strong> and 13.64% and 5.09% were <strong>in</strong>corporated <strong>in</strong> 40.67 kg/1000 m 2 fish<br />
weight ga<strong>in</strong> <strong>in</strong> polyculture system II. Cultivated seaweed could remove up to<br />
10.56% of supplied TN and 9.75% of TP <strong>in</strong> polyculture I, while 10.94% of<br />
supplied TN and 8.83% of TP were <strong>in</strong>corporated seaweed <strong>in</strong> polyculture II. TN<br />
and TP released <strong>in</strong>to environment <strong>in</strong> polyculture I amounted 17.6% and 36.23%,<br />
respectively, and <strong>in</strong> polyculture II 20.6% and 37.41%, respectively. These results<br />
suggest that no significant differences <strong>in</strong> shrimp performance between the two<br />
polyculture <strong>systems</strong> could be observed, additional fish biomass production <strong>in</strong><br />
polyculture II proves the higher <strong>nutrient</strong> retention.<br />
47
Introduction<br />
In recent years the contribution of fish to global diets has reached a record of<br />
about 17 kg per capita on average, supply<strong>in</strong>g over three billion people with at<br />
least 15 percent of their total animal derived prote<strong>in</strong> <strong>in</strong>take (FAO, 2010). Mar<strong>in</strong>e<br />
<strong>aquaculture</strong> has been a rapidly grow<strong>in</strong>g <strong>in</strong>dustry, <strong>in</strong>creas<strong>in</strong>g from about 18.6<br />
million tons <strong>in</strong> 2006 to 20.1 million tons <strong>in</strong> 2009 and these patterns are expected<br />
to cont<strong>in</strong>ue up to the year 2030 due to the <strong>in</strong>creas<strong>in</strong>g global demand and high<br />
market value of <strong>aquaculture</strong> products (FAO, 2010).<br />
There are many obstacles such as diseases, environmental degradation and lack of<br />
management that fish and shrimp farmers <strong>in</strong> Southeast Asia have to overcome<br />
(Primavera, 1998). This means there is an urgent need to develop and dissem<strong>in</strong>ate<br />
<strong>aquaculture</strong> practices <strong>in</strong> an economical yet still environmental friendly manner<br />
(Funge-Smith and Briggs, 1998). One of the ma<strong>in</strong> environmental issues from open<br />
<strong>aquaculture</strong> <strong>systems</strong> is the direct discharge of significant <strong>nutrient</strong> loads <strong>in</strong>to the<br />
environment. Result<strong>in</strong>g waste accumulation generated by the aquatic animal<br />
farm<strong>in</strong>g can be divided <strong>in</strong>to two categories: solid wastes consist<strong>in</strong>g of non-eaten<br />
feed, faecal material, and soluble products which <strong>in</strong>clude ammonia, ur<strong>in</strong>e,<br />
dissolved organic matter and carbon dioxide. In <strong>aquaculture</strong> effluents, about 7-<br />
32% of total nitrogen (TN) and 30-84% of total phosphorus (TP) and up to 27%<br />
of total carbon are bound <strong>in</strong> the particulate fraction and the rema<strong>in</strong>der can be<br />
found <strong>in</strong> dissolved form (Bergheim et al., 1993). Nutrient <strong>in</strong> farm wastes<br />
orig<strong>in</strong>at<strong>in</strong>g from feed supply are of greatest concern due to their role <strong>in</strong><br />
eutrophication processes (Persson, 1991) and discharge should be m<strong>in</strong>imized as<br />
much as possible and viable.<br />
In shrimp <strong>aquaculture</strong>, environmental conditions <strong>in</strong> terms of both quantity and<br />
quality have <strong>in</strong>creas<strong>in</strong>gly become a limit<strong>in</strong>g factor so that the production has<br />
shown a tendency to shift from area-based cultivation (extensive) towards<br />
<strong>in</strong>tensified <strong>systems</strong> (Thakur and L<strong>in</strong>, 2003). The excretion of rema<strong>in</strong><strong>in</strong>g feed<br />
components <strong>in</strong> <strong>in</strong>tensive <strong>systems</strong> will have the potential to degradate<br />
environmental conditions for shrimp culture (Boyd, 1991; Primavera, 1994). The<br />
degradation could cause an oxygen deficiency which <strong>in</strong> turn leads to anaerobic<br />
conditions. In anaerobic conditions, decomposition of organic material will<br />
48
produce toxic compounds, especially ammonia (NH3) and hydrogen sulfide (H2S)<br />
and result<strong>in</strong>g <strong>in</strong> decreased shrimp performance (Boyd, 1991; Goddard, 1996).<br />
One way to improve <strong>aquaculture</strong> production and reduce the negative<br />
environmental impacts is to perform polyculture <strong>systems</strong> that <strong>in</strong>volve organisms<br />
of different trophic levels. Ideally, the <strong>nutrient</strong> <strong>fluxes</strong> <strong>in</strong> the polyculture system<br />
should be balanced with two or more ecologically compatible species, that waste<br />
from one species is recycled to become <strong>in</strong>put (fertilizer or feed) for another<br />
species without conflict<strong>in</strong>g each other (Neori et al., 2000).<br />
In a previous study a comparison of <strong>nutrient</strong> <strong>fluxes</strong> and mass balances between<br />
monoculture and polyculture <strong>systems</strong> us<strong>in</strong>g shrimp and seaweed Gracillaria has<br />
been <strong>in</strong>vestigated (Ihsan et al., submitted). Polyculture <strong>systems</strong>, us<strong>in</strong>g seaweed<br />
and shrimp, act more efficiently with regard to <strong>nutrient</strong> accumulation and system<br />
performance. However, <strong>nutrient</strong> retention is often limited by additional needed<br />
cultivation area, especially if plants are utilized (Buschmann et al., 2001). Thus,<br />
polyculture <strong>systems</strong> us<strong>in</strong>g shrimp and seaweed <strong>in</strong> comb<strong>in</strong>ation with omnivorous<br />
tilapia proposed as a technological alternative for <strong>in</strong>tegrated <strong>aquaculture</strong>. At<br />
present, this study focus on the calculation of <strong>nutrient</strong>s <strong>fluxes</strong> and mass balances<br />
<strong>in</strong> various polyculture <strong>systems</strong> us<strong>in</strong>g shrimp, seaweed and fish <strong>in</strong> order to identify<br />
most efficient polyculture practices.<br />
Material and method<br />
The experiment was conducted <strong>in</strong> Sungai Buntu, West Java over a 90-day period<br />
from July–October 2010 dur<strong>in</strong>g the dry season. This area is located on the<br />
northern Java Island (Figure 1). The experimental site was divided <strong>in</strong>to 3 sectors:<br />
Water <strong>in</strong>put unit of approximately 1 ha, triplicate polyculture I <strong>systems</strong> consist<strong>in</strong>g<br />
of ponds stocked with shrimp and seaweed and triplicate polyculture II <strong>systems</strong><br />
consist<strong>in</strong>g of shrimp + fish + seaweed ponds (Figure 2). The area of each pond<br />
was 1000 m 2 (40 m x 25 m). The water depth of each pond amounted 1 m. Each<br />
pond was fertilized with 3 kg/1000 m 2 of urea before stock<strong>in</strong>g. Fertilizers were<br />
used to activate and <strong>in</strong>crease primary production and establishment of natural<br />
feeds <strong>in</strong> ponds.<br />
49
Location of experiments<br />
(Sungai Buntu-West Java)<br />
Figure 1. Map of Research <strong>Institut</strong>e for Brackish water fisheries, West Java,<br />
Indonesia<br />
Figure 2. Schematic outl<strong>in</strong>e of polyculture <strong>systems</strong> I and II<br />
50
The seaweed, provided from local production <strong>in</strong> Sungai Buntu, Karawang, West<br />
Java was <strong>in</strong>serted <strong>in</strong>to polyethylene ropes that were fixed by rafts. A suspension<br />
culture unit was composed of four rafts, with each <strong>in</strong> turn consisted of n<strong>in</strong>e ropes.<br />
Each rope (about 8.5 m long) was <strong>in</strong>serted with a piece of algae (25 g) every 20<br />
cm. The distance between adjacent ropes and units was 20 cm 3 m, respectively.<br />
Shrimp post larvae (0.43 ± 0.11 g) were stocked <strong>in</strong> each of the 6 ponds at a density<br />
of 15 <strong>in</strong>dividuals/m 2 and seaweed at a density of 0.4 kg/m 2 (Table 2). Triplicate<br />
polyculture II ponds of 1000 m² were additionally stocked with fish (4.7 ± 0.6<br />
g/<strong>in</strong>d) at a density of 0.25 <strong>in</strong>dividuals/m 2 . Before stock<strong>in</strong>g, shrimp and fish were<br />
acclimatized for one night to the pond-water conditions.<br />
Commercial shrimp feed (Lux<strong>in</strong>do 39, Lux<strong>in</strong>do Internusa Ltd.) conta<strong>in</strong><strong>in</strong>g 40%<br />
prote<strong>in</strong> was given. Control sampl<strong>in</strong>g of shrimp weight ga<strong>in</strong> was done every 10<br />
days to determ<strong>in</strong>e the actual weight for feed application. For this procedure 5<br />
<strong>in</strong>dividuals were caught and analyzed. Daily feed supply equaled to 7-10% of<br />
shrimp biomass <strong>in</strong> accordance to time after control sampl<strong>in</strong>g (modified after<br />
Baliao and Tookw<strong>in</strong>as, 2002). At day 0 and day 1 after sampl<strong>in</strong>g, daily feed<br />
supply amounted 7%/shrimp biomass, from day 2 until day 4 8%, from day 5 until<br />
day 7 9% and from day 8 until day 9 10% shrimp biomass were fed. Feed was<br />
given 4 times a day, i.e. at 07.00, 12.00, 17.00 and 22.00. Two percent of the<br />
water volume of the shrimp ponds was exchanged every day.<br />
Sampl<strong>in</strong>g and analytical procedures<br />
Fluxes of follow<strong>in</strong>g water quality parameters were measured: temperature,<br />
sal<strong>in</strong>ity, dissolved oxygen (DO), pH, alkal<strong>in</strong>ity, hydrogen sulphide (H2S), total<br />
suspended solids (TSS), ammonium, nitrate, nitrite, orthophosphate, total nitrogen<br />
(TN) and total phosphorus (TP).<br />
Every 10 days, the water quality was analyzed. Samples of each pond sampl<strong>in</strong>g<br />
po<strong>in</strong>t were taken over 24 hours at 3-hour <strong>in</strong>tervals and pooled for follow<strong>in</strong>g<br />
analytical procedures. Water sample were taken 20 cm below the water surface <strong>in</strong><br />
central pond <strong>in</strong>let and each pond outlet. Every day at 08.00 and 16.00, the water<br />
temperature, sal<strong>in</strong>ity, and dissolved oxygen (DO) were monitored <strong>in</strong> situ us<strong>in</strong>g a<br />
portable (TOA model WQC-20A Electronic Ltd., Japan) water-quality analyzer.<br />
51
Water samples were collected us<strong>in</strong>g plastic bottles attached to the end of a stick.<br />
They were immediately filtered through Whatman GF/F filters 0.7 µM millipore<br />
for soluble <strong>nutrient</strong>s analyses (PO4 -3 , NO3 - , NO2 _ , NH4 + ). The ammonium<br />
concentration <strong>in</strong> the filtrate was measured immediately after filtration. Total<br />
nitrogen (TN), total phosphorus (TP), nitrate, nitrite, and orthophosphate<br />
concentrations were measured us<strong>in</strong>g the APHA (1995) standard methods. The<br />
<strong>nutrient</strong> analyses were performed with a spectrophotometer (Shimadzu UV-2400).<br />
The standard method for determ<strong>in</strong><strong>in</strong>g ammonium, nitrite and nitrate were based<br />
on moderate alkal<strong>in</strong>e solution with hypochlorite, diazotization, and cadmium<br />
reduction followed by diazotization, respectively. The standard method for<br />
determ<strong>in</strong>ation of phosphorus <strong>in</strong> the water and feed and shrimp, seaweed or fish<br />
samples was based on the reaction of ions with an acidified molybdate reagent.<br />
The spectrophotometer wave lengths for ammonium, nitrite, nitrate and<br />
phosphorus were 630 nm, 542 nm, 542 nm, and 882 nm, respectively. GF/F filters<br />
<strong>in</strong> glass dishes were used to determ<strong>in</strong>e suspended solids. Total suspended solids<br />
were estimated us<strong>in</strong>g the standard filtration method (APHA, 1995). H2S was<br />
measured us<strong>in</strong>g the Cl<strong>in</strong>e-method based on N, N-dimethyl-p-phenylenediam<strong>in</strong>e<br />
(Cl<strong>in</strong>e, 1968). The spectrophotometer wave length for H2S was 670 nm. Nitrogen<br />
content <strong>in</strong> the feed, shrimp, fish and seaweed were us<strong>in</strong>g Kjeldahl method.<br />
Calculation<br />
The growth performance criteria of shrimp and fish <strong>in</strong>clud<strong>in</strong>g survival rate,<br />
specific growth rate, and feed conversion ratio were calculated at the end of the<br />
experiment.<br />
Survival Rate (SR) was calculated as a ratio between the shrimp or fish quantity at<br />
sampl<strong>in</strong>g times and stock<strong>in</strong>g time us<strong>in</strong>g the formula:<br />
SR = (Nt / N0) X 100%<br />
With: SR = survival rate<br />
N0 = number of shrimp or fish on day 0 (<strong>in</strong>dividual)<br />
Nt = number of shrimp or fish on day t (<strong>in</strong>dividual)<br />
52
Specific growth rate of shrimp or fish (SGR) represents the relative <strong>in</strong>crease <strong>in</strong><br />
daily weight dur<strong>in</strong>g a certa<strong>in</strong> time <strong>in</strong>terval and were calculated with:<br />
SGR = ((ln Wt - ln W0) / t) X 100%<br />
With: SGR = Specific growth rate<br />
W 0 = weight of shrimp or fish on day-0 (g)<br />
Wt = weight of shrimp or fish on day-t (g)<br />
t = time of experiment (day)<br />
Feed conversion ratio (FCR) is the ratio between the amount of feed given to<br />
shrimp weight ga<strong>in</strong> <strong>in</strong> a certa<strong>in</strong> period (NRC, 1977) us<strong>in</strong>g the formula:<br />
FCR = F / ΔB<br />
With: FCR = feed conversion ratio<br />
F = amount of feed given dur<strong>in</strong>g experiment (kg)<br />
ΔB = shrimp biomass weight ga<strong>in</strong> dur<strong>in</strong>g experiment (kg)<br />
Statistics<br />
Water quality and <strong>nutrient</strong> <strong>fluxes</strong> and growth performance parameter observed<br />
between polyculture I and polyculture II ponds were analyzed statistically. All<br />
data were checked for normality (Kolmogorov-Smirnov test) and homogeneity of<br />
variances (HOV, Brown-Forsythe test). Differences of means of triplicate ponds<br />
(n=3) were evaluated for significance us<strong>in</strong>g the range tests of Tukey HSD<br />
(P
FC : Content of N or P <strong>in</strong> dry pellet<br />
fC : Content of N or P <strong>in</strong> fertilizer<br />
IC : Content of N or P <strong>in</strong> <strong>in</strong>flow<strong>in</strong>g water<br />
SSC : Content of N or P <strong>in</strong> stocked shrimp<br />
SGC : Content of N or P <strong>in</strong> stocked Gracillaria<br />
SFC : Content of N or P <strong>in</strong> stocked fish<br />
HSC : Content of N or P <strong>in</strong> harvested shrimp<br />
HGC : Content of N or P <strong>in</strong> harvested Gracillaria<br />
HFC : Content of N or P <strong>in</strong> harvested fish<br />
OC : Content of N or P <strong>in</strong> outflow<strong>in</strong>g water<br />
Result<br />
Water quality<br />
Table 1 shows that the average concentration of DO <strong>in</strong> polyculture <strong>systems</strong> I and<br />
II as well as of <strong>in</strong>flow<strong>in</strong>g water was <strong>in</strong> high ranges of more than 4 mg/l. The<br />
average concentration of DO between the polyculture <strong>systems</strong> dur<strong>in</strong>g the 90-day<br />
experiment was not significantly different (P>0.05).<br />
Table 1. Mean of water quality parameter over 90 days period (n=3)<br />
Parameter Unit Water <strong>in</strong>put Polyculture I Polyculture II<br />
DO mg/l 4.5 b 5.9 ± 0.7 a 5.4 ± 0.6 a<br />
Sal<strong>in</strong>ity Ppt 27.7 a 29.3 ± 1.0 a 29.9 ± 0.8 a<br />
Température<br />
0 C 27.8 a 26.4 ± 0.05 a 26.9 ± 0.07 a<br />
pH - 7.9 a 8.1 ± 0.1 a 7.9 ± 0.2 a<br />
Alkal<strong>in</strong>ity mg/l 117.6 a 116.4 ± 3.2 a 112.1 ± 2.0 a<br />
H2S mg/l 0 a 0.02 ± 0.001 a 0.03 ± 0.008 a<br />
TSS mg/l 16.3 c 50.5 ± 7.6 a 64.9 ± 4.2 b<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
54
Table 1 shows that the average sal<strong>in</strong>ity for the 90-day experiment was 29.30 ±<br />
1.00 ppt for polyculture I and 29.90 ± 0.80 ppt for polyculture II. Average sal<strong>in</strong>ity<br />
was not significantly different between the ponds (P>0.05).<br />
Figure 3 shows a tendency of alkal<strong>in</strong>ity to decrease dur<strong>in</strong>g the 90-day experiment.<br />
However, the alkal<strong>in</strong>ity was not significantly different between ponds (P>0.05).<br />
Alkal<strong>in</strong>ity <strong>in</strong> polyculture I ranged between 118.93–109.33 mg/l (Figure 3) with an<br />
average of 116.40 ± 3.20 mg/l (Table 1), while <strong>in</strong> polyculture II it ranged between<br />
124.80–102.07 mg/l (Figure 3) with an average of 112.10 ± 2.00 mg/l (Table 1).<br />
The average pH over the 90-day experiment was not significantly different<br />
between polyculture I and II (P>0.05), with 8.10 ± 0.10 for polyculture I and 7.90<br />
± 0.20 for polyculture II (Table 1).<br />
Concentration (mg/l)<br />
140.00<br />
120.00<br />
100.00<br />
80.00<br />
60.00<br />
40.00<br />
20.00<br />
0.00<br />
Alkal<strong>in</strong>ity<br />
a a a a a<br />
a<br />
a a a<br />
a<br />
a a a a a<br />
0 20 40 60 80 100<br />
Time (days)<br />
a a a<br />
ab<br />
b<br />
ab<br />
b<br />
ab<br />
b<br />
Polyculture I<br />
Polyculture II<br />
water <strong>in</strong>put<br />
Figure 3. Concentration of Alkal<strong>in</strong>ity dur<strong>in</strong>g the experimental period, values<br />
are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
55
Concentration (m g/l)<br />
140.00<br />
120.00<br />
100.00<br />
80.00<br />
60.00<br />
40.00<br />
20.00<br />
0.00<br />
Total Suspended Solid<br />
a<br />
a<br />
b<br />
b<br />
b<br />
b<br />
a a b<br />
a<br />
a<br />
a<br />
a<br />
c c c c c c c<br />
0 20 40 60 80 100<br />
a<br />
Time (days)<br />
Figure 4. Concentration of total suspended solid (TSS) dur<strong>in</strong>g the<br />
experimental period, values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
a<br />
a<br />
a<br />
Polyculture I<br />
Polyculture II<br />
water <strong>in</strong>put<br />
TSS tend to <strong>in</strong>crease and was significantly different between polyculture I and II<br />
(P0.05). The average survival rate of shrimp <strong>in</strong> polyculture I dur<strong>in</strong>g the<br />
production period was 84.4%, while <strong>in</strong> polyculture II it was 82.8% (Table 2.). The<br />
data showed that mortality rates were low <strong>in</strong> both <strong>systems</strong>. Survival rate of fish <strong>in</strong><br />
polyculture II at harvest amounted 78.8% (Table 2).<br />
56
Table 2. Performance of experimental polyculture system over 90 days period<br />
(n=3)<br />
Parameter Polyculture I Polyculture II<br />
Stock<strong>in</strong>g density:<br />
Shrimp (<strong>in</strong>dividual/m2)<br />
Fish (<strong>in</strong>dividual/m2)<br />
Total larvae stocked:<br />
Shrimp (<strong>in</strong>d)<br />
Fish (<strong>in</strong>d)<br />
Weight of stocked larvae:<br />
Shrimp (g/<strong>in</strong>d)<br />
Fish (g/<strong>in</strong>d)<br />
Total weight:<br />
Shrimp (kg)<br />
Fish (kg)<br />
15<br />
-<br />
15000<br />
-<br />
0.43 ± 0.11 a<br />
-<br />
6.45 a<br />
-<br />
15<br />
0.25<br />
15000<br />
250<br />
0.43 ± 0.11 a<br />
4.7 ± 0.6<br />
6.45 a<br />
1.18<br />
Area (m2) 1000 1000<br />
Culture time (days) 90 90<br />
Total Feed (kg) 526.65 a 526.65 a<br />
At harvest:<br />
Shrimp (<strong>in</strong>d/m2)<br />
Fish (<strong>in</strong>d/m2)<br />
Weight:<br />
Shrimp (g/<strong>in</strong>d)<br />
Fish (g/<strong>in</strong>d)<br />
Total weight:<br />
Shrimp (kg/1000 m 2 )<br />
Fish (kg/1000 m 2 )<br />
12.66 a<br />
-<br />
24.73 ± 0.71 a<br />
-<br />
313.08 a<br />
-<br />
12.42 a<br />
0.20<br />
23.45 ± 1.43 a<br />
206.1 ± 11.36<br />
291.25 a<br />
40.67<br />
Survival rate<br />
Shrimp (%)<br />
84.4<br />
Fish (%)<br />
a<br />
82.8 a<br />
78.8<br />
FCR 1.72 a 1.84 a<br />
57
SGR:<br />
Shrimp (%/day)<br />
Fish (%/day)<br />
4.5 a<br />
4.4 a<br />
4.2 a<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
Figure 5 shows that the growth rate of shrimp was not significantly different<br />
between polyculture I and II (P>0.05). The average weight of shrimp at harvest<br />
was 24.73 ± 0.71 and 23.45 ± 1.43 g/<strong>in</strong>d for polyculture I and II, respectively<br />
(Table 2), while the average fish weight at the time of harvest was 206.1 ± 11.36<br />
g/<strong>in</strong>d (Table 2). Specific growth rate (SGR) for shrimp <strong>in</strong> polyculture I and II was<br />
not significantly different (P>0.05) with an average value over the 90-day<br />
experiment of 4.5%/day and 4.4%/day, respectively. SGR of fish over the 90-day<br />
period amounted 4.2% /day.<br />
Weight (g)<br />
30.00<br />
25.00<br />
20.00<br />
15.00<br />
10.00<br />
5.00<br />
0.00<br />
Weight<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a<br />
0 20 40 60 80 100<br />
a<br />
Time (days)<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a<br />
Polyculture I<br />
Polyculture II<br />
Figure 5. Individual weight of shrimp dur<strong>in</strong>g the experimental period, values<br />
are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
58
Biomass production of shrimp <strong>in</strong> polyculture I and II was not significantly<br />
different (P>0.05) with an average value of 313.08 and 291.25 kg/1000 m 2 ,<br />
respectively (Table 2). In polyculture II there was an additional production from<br />
the fish of 40.67 kg/1000 m 2 (Table 2).<br />
Nutrient flux<br />
The ammonium concentration <strong>in</strong>creased gradually <strong>in</strong> both polyculture <strong>systems</strong><br />
and orthophosphate concentration <strong>in</strong>creased progressively as well. Even though<br />
well water was supplied to the pond at a renewal rate of 2%/day, the ammonium<br />
concentrations <strong>in</strong> polyculture I <strong>in</strong>creased dur<strong>in</strong>g the production period from 0.12<br />
to 0.53 mg/l (Figure 6), with an average concentration of 0.34 ± 0.06 mg/l (Table<br />
3). In the polyculture II system, it <strong>in</strong>creased from 0.17 to 0.71 mg/l (Figure 6),<br />
with an average over the production period of 0.45 ± 0.07 mg/l. Therefore,<br />
ammonium concentrations <strong>in</strong> both polyculture <strong>systems</strong> did not display significant<br />
differences (P>0.05).<br />
Concentration (mg/l)<br />
0.800<br />
0.700<br />
0.600<br />
0.500<br />
0.400<br />
0.300<br />
0.200<br />
0.100<br />
0.000<br />
a<br />
a<br />
a b<br />
a<br />
c c c c<br />
a a a a<br />
Ammonium<br />
a a b<br />
c<br />
0 20 40 60 80 100<br />
Time (days)<br />
a<br />
b<br />
a<br />
b<br />
c c c c<br />
Figure 6. Concentration of ammonium-nitrogen (NH4 - -N) dur<strong>in</strong>g the<br />
experimental period, values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
59<br />
a<br />
a<br />
Polyculture I<br />
Polyculture II<br />
Water <strong>in</strong>put
Concentration (mg/l)<br />
0.080<br />
0.070<br />
0.060<br />
0.050<br />
0.040<br />
0.030<br />
0.020<br />
0.010<br />
0.000<br />
a<br />
a<br />
a a<br />
c c<br />
a<br />
a<br />
a<br />
c c<br />
Orthophosphate<br />
b<br />
a<br />
c c c c c<br />
0 20 40 60 80 100<br />
b<br />
a<br />
Time (days)<br />
b<br />
a<br />
b<br />
a<br />
b<br />
a<br />
b<br />
Polyculture I<br />
Polyculture II<br />
Water <strong>in</strong>put<br />
Figure 7. Concentration of orthophosphate (PO4-P) dur<strong>in</strong>g the experimental<br />
period, values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
Orthophosphate <strong>in</strong> polyculture I <strong>in</strong>creased dur<strong>in</strong>g the 90-day period from 0.01 to<br />
0.05 mg/l (Figure 7), with an average concentration of orthophosphate of 0.03 ±<br />
0.006 mg/l (Table 3), while <strong>in</strong> polyculture II it <strong>in</strong>creased from 0.01 to 0.07 mg/l<br />
(Figure 7) with an average of 0.04 ± 0.003 mg/l. These concentrations <strong>in</strong> both<br />
polyculture <strong>systems</strong> did not exhibit significant differences (P>0.05).<br />
Nitrite (NO2 - ) and nitrate (NO3 - ) <strong>in</strong> both polyculture <strong>systems</strong> did not show<br />
significant differences (P>0.05) with average concentrations of 0.005 ± 0.001<br />
mg/l and 0.05 ± 0.01, mg/l <strong>in</strong> polyculture I and 0.006 ± 0.001 mg/l and 0.05 ±<br />
0.007 mg/l <strong>in</strong> polyculture II, respectively (Table 3).<br />
60
Table 3. Mean of <strong>nutrient</strong> concentrations over 90 days period (n=3)<br />
Variable Unit Water <strong>in</strong>put Polyculture I Polyculture II<br />
NH4 mg/l 0.014 b 0.34 ± 0.06 a 0.45 ± 0.07 a<br />
NO2 mg/l 0.0002 b 0.005 ± 0.001 a 0.006 ± 0.001 a<br />
NO3 mg/l 0.004 b 0.05 ± 0.01 a 0.05 ± 0.007 a<br />
PO4 mg/l 0.01 b 0.03 ± 0.006 a 0.04 ± 0.003 a<br />
TN mg/l 0.18 b 2.25 ± 0.4 a 2.66 ± 0.8 a<br />
TP mg/l 0.046 b 0.84 ± 0.05 a 0.89 ± 0.05 a<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
Additionally, total nitrogen (TN) and total phosphorus (TP) concentration<br />
<strong>in</strong>creased <strong>in</strong> the outlet water of polyculture <strong>systems</strong> I and II. TN <strong>in</strong> the polyculture<br />
I pond <strong>in</strong>creased from 0.40–5.15 mg/l (Figure 8), with an average of 2.25 ± 0.40<br />
mg/l (Table 3) and TN <strong>in</strong> polyculture II ranged from 0.47–6.16 mg/l (Figure 8),<br />
with an average of 2.66 ± 0.80 mg/l (Table 3). TP <strong>in</strong> polyculture I <strong>in</strong>creased from<br />
0.03–1.56 mg/l (Figure 9), with an average of 0.84 ± 0.05 mg/l (Table 3), while <strong>in</strong><br />
polyculture II values of 0.03–1.64 mg/l (Figure 9) and an average of 0.89 ± 0.05<br />
mg/l (Table 3) could be observed, but no significant differences (P>0.05) could be<br />
calculated between the <strong>systems</strong>.<br />
61
Concentration (m g/l)<br />
Concentration (mg/l)<br />
8.000<br />
7.000<br />
6.000<br />
5.000<br />
4.000<br />
3.000<br />
2.000<br />
1.000<br />
0.000<br />
Total Nitrogen (TN)<br />
a<br />
b a<br />
a<br />
a<br />
b<br />
a<br />
b a<br />
a<br />
a<br />
b<br />
a<br />
b<br />
a<br />
b<br />
a<br />
0 20 40 60 80 100<br />
a<br />
Time (days)<br />
a<br />
a<br />
a a<br />
a<br />
b b b<br />
a<br />
Polyculture I<br />
Polyculture II<br />
Water <strong>in</strong>put<br />
Figure 8. Concentration of total nitrogen (TN) dur<strong>in</strong>g the experimental<br />
period, values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
1.800<br />
1.600<br />
1.400<br />
1.200<br />
1.000<br />
0.800<br />
0.600<br />
0.400<br />
0.200<br />
0.000<br />
Total Phosphorus (TP)<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a<br />
b<br />
a<br />
b b b b b b b<br />
0 20 40 60 80 100<br />
Time (days)<br />
a<br />
Polyculture I<br />
Polyculture II<br />
water <strong>in</strong>put<br />
Figure 9. Concentration of total phosphorus (TP) dur<strong>in</strong>g the experimental<br />
period, values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
62
Mass balance<br />
Total nitrogen (TN) and total phosphorus (TP) from fertilizer amounted 1.56<br />
kg/1000 m 2 and 0.2 kg/1000 m 2 for polyculture system I and II, respectively.<br />
Whereas TN and TP from <strong>in</strong>flow<strong>in</strong>g water were 0.5 kg/1000 m 2 and 0.13 kg/1000<br />
m 2 for both polyculture <strong>systems</strong> (Figure 10 and 11).<br />
TN-mass balance polyculture system I<br />
Figure 11. Total nitrogen mass balance <strong>in</strong> experimental polyculture and<br />
Valueare mean of triplicate ponds (n=3)<br />
Fertilization<br />
4.36% Values (1.56 kg) with the same superscript letter do not differ Pond significantly Water between<br />
polyculture <strong>systems</strong> I and II (P>0.05).<br />
a<br />
06%<br />
(0.02 kg) a<br />
ssociated<br />
25.06%<br />
(8.97 kg) a<br />
0.<br />
a<br />
Fertilization<br />
4.36% (1.56 kg) Pond Water<br />
a<br />
06%<br />
(0.02 kg) a<br />
ssociated<br />
25.06%<br />
(8.97 kg) a<br />
0.<br />
a<br />
Water <strong>in</strong>flow<br />
1.4%<br />
(0.5 kg) a<br />
Water <strong>in</strong>flow<br />
1.4%<br />
(0.5 kg) a<br />
Seaweed stocked<br />
0.06%<br />
(0.02 kg)<br />
rimp stocked<br />
a<br />
Seaweed stocked<br />
0.06%<br />
(0.02 kg)<br />
Shrimp<br />
stocked<br />
a<br />
Sh<br />
Shrimp feed<br />
94.13%<br />
(33.7 kg) a<br />
Shrimp feed<br />
94.13%<br />
(33.7 kg) a<br />
TN-mass balance polyculture system II<br />
Fertilization<br />
4.34% (1.56 kg) a<br />
Seaweed stocked<br />
0.06%<br />
(0.02 kg)<br />
Shrimp stocked<br />
0.06%<br />
(0.02 kg)<br />
a<br />
Fish stocked<br />
0.36%<br />
(0.13 kg)<br />
Shrimp<br />
0.06%<br />
(0.02 kg) a<br />
Fish stocked<br />
0.36%<br />
(0.13 kg) b<br />
Fertilization<br />
4.34% (1.56 kg) a<br />
Seaweed stocked<br />
0.06%<br />
(0.02 kg)<br />
Shrimp stocked<br />
0.06%<br />
(0.02 kg)<br />
a<br />
Fish stocked<br />
0.36%<br />
(0.13 kg)<br />
Shrimp<br />
0.06%<br />
(0.02 kg) a<br />
Fish stocked<br />
0.36%<br />
(0.13 kg) b<br />
Shrimp feed<br />
93.79% (33.7 kg) a<br />
Shrimp feed<br />
93.79% (33.7 kg) a<br />
Shrimp harvest<br />
46.79% (16.75 kg) a<br />
Shrimp harvest<br />
46.79% (16.75 kg) a<br />
Shrimp harvest<br />
41.47% (14.9 kg) a<br />
Shrimp harvest<br />
41.47% (14.9 kg) a<br />
Seaweed harvest<br />
10.56% (3.78 kg) a<br />
Seaweed harvest<br />
10.56% (3.78 kg) a<br />
Seaweed harvest<br />
10.94% (3.93 kg) a<br />
Seaweed harvest<br />
10.94% (3.93 kg) a<br />
Pond Water<br />
Others<br />
Outlet water<br />
17.6%<br />
(6.3 kg) a<br />
Outlet water<br />
17.6%<br />
(6.3 kg) a<br />
Fish harvest<br />
13.64%<br />
(4.9 kg) b<br />
Fish harvest<br />
13.64%<br />
(4.9 kg) b<br />
Others<br />
associated<br />
13.36%<br />
(4.8 kg) b<br />
Others<br />
associated<br />
13.36%<br />
(4.8 kg) b<br />
Outlet<br />
water<br />
20.6%<br />
(7.4 kg) a<br />
Outlet<br />
water<br />
20.6%<br />
(7.4 kg) a<br />
Figure 10. Total nitrogen mass balance <strong>in</strong> experimental polyculture <strong>systems</strong><br />
I and II. Values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly between polyculture<br />
<strong>systems</strong> I and II (P>0.05).<br />
63
TP-mass balance polyculture system I<br />
Shrimp stocked<br />
0.15%<br />
(0.01 kg) a<br />
Seaweed Stocked<br />
0.15%<br />
(0.01 kg) a<br />
Shrimp stocked<br />
0.15%<br />
(0.01 kg) a<br />
Seaweed Stocked<br />
0.15%<br />
(0.01 kg) a<br />
Fertilization<br />
3% (0.2 kg) a<br />
Fertilization<br />
3% (0.2 kg) a<br />
Water <strong>in</strong>flow<br />
1.95% (0.13 kg) a<br />
Water <strong>in</strong>flow<br />
1.95% (0.13 kg) a<br />
Shrimp feed<br />
94.75% (6.32 kg) a<br />
Shrimp feed<br />
94.75% (6.32 kg) a<br />
TP-mass balance polyculture system II<br />
Stocked shrimp<br />
0.15%<br />
(0.01 kg) a<br />
Seaweed stocked<br />
0.15%<br />
(0.01 kg) a<br />
Fish stocked<br />
0.18%<br />
(0.012 kg) b<br />
Stocked shrimp<br />
0.15%<br />
(0.01 kg) a<br />
Seaweed stocked<br />
0.15%<br />
(0.01 kg) a<br />
Fish stocked<br />
0.18%<br />
(0.012 kg) b<br />
Fertilization<br />
2.99% (0.2 kg) a<br />
Fertilization<br />
2.99% (0.2 kg) a<br />
Water <strong>in</strong>flow<br />
1.95%<br />
(0.13 kg) a<br />
Water <strong>in</strong>flow<br />
1.95%<br />
(0.13 kg) a<br />
Shrimp feed 94.58%<br />
(6.32 kg) a<br />
Shrimp feed 94.58%<br />
(6.32 kg) a<br />
Shrimp harvest<br />
14.99% (1.0 kg) a<br />
Shrimp harvest<br />
14.99% (1.0 kg) a<br />
Shrimp harvest<br />
13.47% (0.90 kg) a<br />
Shrimp harvest<br />
13.47% (0.90 kg) a<br />
Seaweed harvest<br />
9.75% (0.65 kg) a<br />
Seaweed harvest<br />
9.75% (0.65 kg) a<br />
Pond Water<br />
Seaweed harvest<br />
8.83% (0.59 kg) a<br />
Seaweed harvest<br />
8.83% (0.59 kg) a<br />
Pond Water<br />
Others<br />
Associated<br />
40.03%<br />
(2.67 kg) a<br />
Others<br />
Associated<br />
40.03%<br />
(2.67 kg) a<br />
Outlet<br />
water<br />
35.23%<br />
(2.35 kg) a<br />
Outlet<br />
water<br />
35.23%<br />
(2.35 kg) a<br />
Fish harvest<br />
5.09%<br />
(0.34 kg) b<br />
Fish harvest<br />
5.09%<br />
(0.34 kg) b<br />
Others<br />
associated<br />
35.20%<br />
(2.35 kg) b<br />
Others<br />
associated<br />
35.20%<br />
(2.35 kg) b<br />
Outlet<br />
water<br />
37.41%<br />
(2.50 kg) a<br />
Outlet<br />
water<br />
37.41%<br />
(2.50 kg) a<br />
Figure 11. Total phosphate mass balance <strong>in</strong> experimental polyculture<br />
<strong>systems</strong> I and II. Values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly between polyculture<br />
<strong>systems</strong> I and II (P>0.05).<br />
In polyculture system I shrimp yielded a growth performance of 0.31 kg/m 2 and a<br />
feed conversion ratio (FCR) of 1.72, and <strong>in</strong> polyculture system II equal<br />
performance with 0.29 kg/m 2 but additional 0.04 kg fish/m 2 , at FCR of 1.84.<br />
64
Shrimp and seaweed harvested <strong>in</strong> polyculture system I <strong>in</strong>corporated <strong>in</strong> total at<br />
least 57.35% of TN and 24.74% of TP and <strong>in</strong> polyculture system II higher but no<br />
significantly different (P>0.05) <strong>nutrient</strong> assimilation of 66.05% for TN and of<br />
27.39% for TP could be found <strong>in</strong> the total biomass (shrimp, seaweed and fish).<br />
Total nitrogen and phosphorous released with the outlet water amounted 6.3<br />
kg/1000 m 2 and 2.35 kg/1000 m 2 <strong>in</strong> polyculture system I. In the polyculture<br />
system II, 7.4 kg/1000 m 2 and 2.50 kg/1000 m 2 of TN and TP could be found <strong>in</strong><br />
the outflow<strong>in</strong>g water, but no significant differences (P>0.05) could be calculated<br />
between the <strong>systems</strong>.<br />
The largest source of TN orig<strong>in</strong>ated from feed with 94.13% for the polyculture<br />
system I and 93.79% for the polyculture system II. The rema<strong>in</strong><strong>in</strong>g nitrogen<br />
derived from fertilizer and <strong>in</strong>flow<strong>in</strong>g water with 4.36% and 1.4% <strong>in</strong> polyculture<br />
system I and with 4.34% and 1.39% <strong>in</strong> polyculture system II (Figure 10). In this<br />
model, the amount of TN from stocked shrimp larvae and seaweed <strong>in</strong> polyculture<br />
system I was 0.02 kg/1000 m 2 and 0.02 kg/1000 m 2 , respectively. This means<br />
only 0.12% of TN <strong>in</strong> the ponds derived from stocked biomass <strong>in</strong> polyculture<br />
system I. In polyculture system II 0.06% and 0.36 % of TN derived from stocked<br />
seaweed and fish (Figure 10).<br />
Outlet water conta<strong>in</strong>ed 17.6% of TN for the polyculture system I and 20.6% for<br />
the polyculture system II (Figure 10). 25.06% of TN <strong>in</strong> polyculture system I could<br />
be analyzed as unidentified losses and 13.36% <strong>in</strong> polyculture system II.<br />
With 94.75% for the polyculture system I and 94.58% for the polyculture system<br />
II largest source of total phosphorus (TP) orig<strong>in</strong>ated from feed, but without<br />
significant differences (P>0.05) between the <strong>systems</strong>. The rema<strong>in</strong><strong>in</strong>g TP derived<br />
from fertilizer and <strong>in</strong>flow<strong>in</strong>g water with around 3% and 1.95% for both<br />
polyculture <strong>systems</strong>. TP orig<strong>in</strong>ated from stocked shrimp larvae and seaweed were<br />
0.15% and 0.15% for both polyculture <strong>systems</strong>. TP from stocked fish amounted<br />
0.18% <strong>in</strong> polyculture system II. Total phosphorus (TP) <strong>in</strong> outlet water was 2.35<br />
kg/1000m² for the polyculture system I and 2.50 kg/1000m² for the polyculture<br />
system II (Figure 11). That means, 35.23% of TP <strong>in</strong>put for the polyculture system<br />
I and 37.41% of TP for the polyculture system II were discharged to the<br />
environment, but no significant differences (P>0.05) could be calculated between<br />
65
the <strong>systems</strong>. 40.03% and 35.20% of TP <strong>in</strong> polyculture system I and II were<br />
unaccounted and significant differences (P0.05). It can<br />
be stated that the utilization of feed by shrimp <strong>in</strong> polyculture I and II was efficient<br />
for growth performance. In comparison to the global average shrimp feed<br />
conversion ratio of around 2.0 (Tacon, 2002), the observed feed conversions <strong>in</strong><br />
both polyculture <strong>systems</strong> were very efficient.<br />
In general, the presence of fish led to lower dissolved oxygen (DO) <strong>in</strong> polyculture<br />
II than <strong>in</strong> polyculture I even though it was not significantly different (P>0.05)<br />
(Table 1). In both polyculture <strong>systems</strong>, aeration was used every night from 22.00<br />
until 05.00. Hydrogen sulphide (H2S) concentration for 90 days was still with<strong>in</strong><br />
the limits. The average of H2S for polyculture I and II were 0.02 ± 0.001 and 0.03<br />
± 0.008 mg/l (Table 1), respectively. At levels of 0.1–0.2 mg/l H2S <strong>in</strong> the water,<br />
shrimp growth will be <strong>in</strong>fluenced and they will die <strong>in</strong>stantly at concentrations<br />
66
higher than 4 mg/l (Law, 1988). Thus, DO concentration and H2S for the 90-day<br />
period were still with<strong>in</strong> the safe limits for shrimp and fish. Additionally DO<br />
concentrations should be l<strong>in</strong>ked with seaweed assimilation activities. Its<br />
photosynthesis produces DO that promotes decomposition of organics (Xu, 2008).<br />
The fish <strong>in</strong> studied polyculture system impacted the amount of suspended solids<br />
by faecal excretion and bioturbation, so that amount of total suspended solids<br />
(TSS) <strong>in</strong> polyculture II was higher than <strong>in</strong> polyculture I (P
study showed that seaweed can remove 3.5% of <strong>in</strong>flow<strong>in</strong>g TN and 2.4% of<br />
<strong>in</strong>flow<strong>in</strong>g TP (Ihsan et al., submitted). In addition, ammonium <strong>in</strong> polyculture was<br />
lower than <strong>in</strong> monoculture <strong>systems</strong> and amounted 0.24 mg/l while <strong>in</strong> monoculture<br />
0.37 mg/l could be analyzed. Troell et al. (1997) reported that seaweed have a<br />
high capacity for remov<strong>in</strong>g <strong>nutrient</strong>s from fish effluents, and seaweed production<br />
is higher <strong>in</strong> areas surround<strong>in</strong>g fish cage than <strong>in</strong> areas apart from <strong>aquaculture</strong><br />
<strong>systems</strong>. Seaweed had the potential to remove at least 5% of dissolved nitrogen<br />
released from the fish farm and 7% of released dissolved phosphorous.<br />
Buschmann et al. (1994) found that tank cultivated Gracillaria could remove as<br />
much as 90-95% of the ammonium <strong>in</strong> effluent waters released from salmon tanks.<br />
In this study, <strong>nutrient</strong> assimilation by seaweed between the two polyculture<br />
<strong>systems</strong> did not result <strong>in</strong> significant differences (Figures 10 and 11). Our results<br />
showed a high capacity <strong>in</strong> assimilation of excretory products from shrimp<br />
<strong>nutrient</strong>s by seaweed <strong>in</strong> both polyculture <strong>systems</strong>. The ability of Gracillaria to<br />
assimilate and store nitrogen for ubsequent growth makes it possible to utilize<br />
high <strong>nutrient</strong> concentrations most efficiently. Such rapid accumulation by<br />
seaweed has been documented to function even <strong>in</strong> darkness (Cohen and Neori,<br />
1991)<br />
Mass balance model calculated <strong>in</strong> this study demonstrate <strong>nutrient</strong> utilization <strong>in</strong> the<br />
evaluated polyculture <strong>systems</strong>. TN and TP <strong>in</strong>corporated <strong>in</strong> shrimp and seaweed <strong>in</strong><br />
polyculture I was lower than polyculture <strong>systems</strong> II but not significantly different<br />
(Figures 10 and 11). Nutrients were efficiently utilized by shrimp, seaweed and<br />
fish. In comparison to previous results 34.3% of TN and 9.3% of TP were<br />
<strong>in</strong>corporated <strong>in</strong> shrimp and Gracillaria of polyculture <strong>systems</strong> while <strong>in</strong><br />
monoculture only 24.2% of TN and 5.3% of TP were reta<strong>in</strong>ed <strong>in</strong> shrimp (Ihsan et<br />
al., submitted). Neori et al. (1998) reported that the seaweed harvest conta<strong>in</strong>ed<br />
about 33% of the total N <strong>in</strong>put and 50% was fed to the animal <strong>in</strong> the overall N<br />
budget of the abalone tanks and their seaweed biofilter tanks. Lombardi et al.<br />
(2006) reported that shrimp harvest<strong>in</strong>g accounted for 35.5% and 6.1% of the total<br />
nitrogen and total phosphorus <strong>in</strong>put <strong>in</strong>to the ponds <strong>in</strong> cage polyculture of white<br />
shrimp with seaweed Kappaphycus alvarezii.<br />
68
TN and TP <strong>in</strong>corporated <strong>in</strong> organism <strong>in</strong> polyculture system I were higher than <strong>in</strong><br />
polyculture system II, while TN and TP discharged to the environment through<br />
outlet water <strong>in</strong> both polyculture <strong>systems</strong> did not differ significantly (Figure 10 and<br />
11). Previous results (Ihsan et al., submitted) reported that 44.4% of TN and of<br />
43.3% TP <strong>in</strong> polyculture <strong>systems</strong> and 50.4% of TN and 42.8% of TP <strong>in</strong><br />
monoculture <strong>systems</strong> were <strong>in</strong>corporated <strong>in</strong> organic biomass, whereas 21.3% and<br />
47.3% of TN and TP were released <strong>in</strong>to the environment <strong>in</strong> polyculture system <strong>in</strong><br />
contrast to 25.4% and 51.9% TN and TP released from monoculture <strong>systems</strong>,<br />
respectively. Lombardi et al. (2006) reported that outlet water removed significant<br />
quantities of nitrogen (36.7%) and phosphorus (30.3%) <strong>in</strong> cage polyculture of the<br />
white shrimp and seaweed Kappaphycus alvarezii. Neori and Shpigel (1999)<br />
recorded a reduction <strong>in</strong> the effluent of 72% of total nitrogen and 61% of total<br />
phosphorus <strong>in</strong> <strong>in</strong>tegrated culture of prawn (Penaeus monodon), mussel (Mytilus<br />
edulis) and seaweed Gracillaria. In polyculture system, TN and other excess<br />
<strong>nutrient</strong>s from the feed based shrimp culture are taken up by seaweed (Mart<strong>in</strong>ez-<br />
Aragon et al., 2002). A primary role of biofiltration is the treatment and<br />
conversion of toxic metabolites and pollutants. Microalgae photosynthetically<br />
convert the dissolved <strong>in</strong>organic <strong>nutrient</strong>s <strong>in</strong>to particulate matter suspended <strong>in</strong> the<br />
water, while seaweed <strong>in</strong> contrast extract the <strong>nutrient</strong>s out of the water (Troell and<br />
Norberg, 1998). Seaweed efficiently take up dissolved <strong>in</strong>organic nitrogen present<br />
<strong>in</strong> fish net pen effluents (Troell et al., 1999). Seaweed growth on polyculture<br />
effluents has been also shown to be superior than <strong>in</strong> fertilizer enriched seawater<br />
(Neori et al., 1991).<br />
Total nitrogen (TN) and total phosphorus (TP) <strong>in</strong>corporated <strong>in</strong> shrimp <strong>in</strong> this<br />
study did not show significant differences (P>0.05). From the above it can be<br />
stated that the rate of feed utilization by shrimp was optimal, as well as the ability<br />
of seaweed Gracillaria and fish to utilize <strong>nutrient</strong>s <strong>in</strong> the pond. This proves the<br />
use of polyculture <strong>in</strong> <strong>aquaculture</strong> <strong>systems</strong> <strong>in</strong> order to improve <strong>nutrient</strong> utilization<br />
and to decrease <strong>nutrient</strong> discharge to the environment. However, despite this<br />
relative success, it is necessary to exam<strong>in</strong>e other polyculture <strong>systems</strong> by<br />
<strong>in</strong>tegration of other species such as oysters with seaweed, shrimp and fish to<br />
enhance the <strong>systems</strong> <strong>nutrient</strong> assimilation performance.<br />
69
Conclusion<br />
This study showed that polyculture with shrimp (Penaeus vannamei), fish (Tilapia<br />
sp), and seaweed Gracillaria can be used to <strong>in</strong>crease biomass production.<br />
Inflow<strong>in</strong>g <strong>nutrient</strong>s can be used either by shrimp (Penaeus vannamei), fish<br />
(Tilapia sp) or seaweed Gracillaria (Gracillaria verrucosa). The ability of<br />
seaweed Gracillaria to do photosynthesis caused optimal levels of dissolved<br />
oxygen (DO). The impact of fish as a co-culture organism caused higher total<br />
suspended solids (TSS) <strong>in</strong> polyculture II than <strong>in</strong> polyculture I, but it was still<br />
with<strong>in</strong> the safe limits for shrimp.<br />
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susta<strong>in</strong>able <strong>in</strong>tegrated mariculture. World Aquacult. 30:46-9,51.<br />
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shrimp <strong>aquaculture</strong>. Report prepared under the World Bank, NACA,<br />
WWF, and FAO consortium program on shrimp farm<strong>in</strong>g and the<br />
environment. Published by consortium. 69.<br />
Thakur, D. P. And C. K. L<strong>in</strong>. 2003. Water quality and <strong>nutrient</strong> budget <strong>in</strong> closed<br />
shrimp (Penaeus monodon) culture system. Aquaculture eng<strong>in</strong>eer<strong>in</strong>g. 27.<br />
159-176.<br />
Troell, M. and Norberg, J. 1998. Modell<strong>in</strong>g output and retention of suspended<br />
solid <strong>in</strong> an <strong>in</strong>tegrated salmon-mussel culture. Ecol. Model. 110:65-77.<br />
Troell, M., C Hall<strong>in</strong>g, A Nilsson, A. H Buschmann., N Kautsky, L Kautsky. 1997.<br />
Integrated mar<strong>in</strong>e cultivation of Gracillaria chilensis (Gracilariales,<br />
72
Bangiophyceae) and salmon cages for reduced environmental impact and<br />
<strong>in</strong>creased economic output. Aquaculture 156:45–61.<br />
Xu, Y. J., J. Fang, Q. Tang, J. L<strong>in</strong>, G. Le. 2008. Improvement of water quality by<br />
the macroalga, Gracillaria lemaneiformis (Rhodophyta), near <strong>aquaculture</strong><br />
effluent outlets. World <strong>aquaculture</strong> society. 39. 549-555.<br />
Yang, Y. F., X. G. Fei, J. M. Song, H. Y. Hu, G. C. Wang, Kyo, Chung. 2006.<br />
Growth of Gracillaria lemaneiformis under different cultivation conditions<br />
and its effects on <strong>nutrient</strong> removal <strong>in</strong> Ch<strong>in</strong>ese coastal waters. Aquaculture.<br />
254 (1-4). 248-255.<br />
73
Chapter 4: Nitrogen Assimilation Potential of Seaweed<br />
(Gracillaria verrucosa) <strong>in</strong> Polyculture with Pacific White Shrimps<br />
(Penaeus vannamei)<br />
Y. N. Ihsan ab , K. J. Hesse c , C. Schulz ab<br />
a Gesellschaft <strong>für</strong> Mar<strong>in</strong>e Aquakultur mbH, Hafentörn 3, D-25761 Büsum<br />
b <strong>Institut</strong>e for Animal Breed<strong>in</strong>g and Husbandry, Christian-Albrechts-Universität<br />
D-24098 Kiel<br />
c Research and Technology Centre, Christian-Albrechts-Universität<br />
D-25761 Büsum<br />
Submitted to the Journal of Asian Fisheries Society<br />
74
Abstract<br />
In order to evaluate the <strong>nutrient</strong> absorption efficiency of comb<strong>in</strong>ed shrimp and<br />
seaweed production, nitrogen <strong>fluxes</strong> <strong>in</strong> polycultures were compared with shrimp<br />
monoculture <strong>systems</strong>. Therefore, triplicate concrete tanks, with a volume of 3 m 3 ,<br />
were stocked with shrimp Penaeus vannamei (6–7 g, 5 <strong>in</strong>d/100 litres) and<br />
seaweed (Gracillaria verrucosa) <strong>in</strong> densities of 0 g/l, 3.125 g/l, 6.250 g/l, and<br />
9.375 g/l. The culture period lasted four weeks and water samples were taken<br />
every week to measure <strong>nutrient</strong> <strong>fluxes</strong>. The use of seaweed at a density of 3.125<br />
g/l <strong>in</strong> shrimp polyculture showed the highest ability for nitrogen assimilation<br />
orig<strong>in</strong>at<strong>in</strong>g from shrimp waste. This treatment <strong>in</strong>creased shrimp survival rate from<br />
63% (without seaweed) to 83% and the growth performance of shrimp from<br />
247.78 g (without seaweed) to 350.20 g. Rema<strong>in</strong><strong>in</strong>g nitrogen excreted by shrimp<br />
amounted to 15.36 g, which was ma<strong>in</strong>ly (14.62 g) utilized by seaweed to form a<br />
biomass of 16.90 kg. Therefore, polyculture <strong>systems</strong> us<strong>in</strong>g seaweed seem to act<br />
more efficiently with regard to <strong>nutrient</strong> accumulation.<br />
75
Introduction<br />
Shrimp <strong>aquaculture</strong> has developed quickly s<strong>in</strong>ce the 1980s <strong>in</strong> Southeast Asian<br />
countries <strong>in</strong>clud<strong>in</strong>g Indonesia. However, the rapid <strong>in</strong>dustrial growth of<br />
<strong>aquaculture</strong> has raised environmental concerns about eutrophication and depletion<br />
of natural habitats (Naylor et al., 2000; Zhang, 2003; Zhou et al., 2003; Mao et al.,<br />
2006). Animal mariculture and other anthropogenic activities generate large<br />
quantities of organic and <strong>in</strong>organic waste. Especially feed supply results <strong>in</strong><br />
excretory products and discharge of uneaten feed, which releases up to 70% of<br />
dietary <strong>nutrient</strong>s <strong>in</strong>to the environment (Porter et al., 1987). Released <strong>nutrient</strong>s<br />
<strong>in</strong>crease eutrophication processes (Neori et al., 1991; Rathakrishnan, 2001) and<br />
the accumulation of acute toxic substances for aquatic animals (Troell et al., 1999;<br />
Neori et al., 2001).<br />
Integrated <strong>multitrophic</strong> <strong>aquaculture</strong> techniques are good candidates to overcome<br />
these susta<strong>in</strong>ability problems (Ruddle and Zong, 1988; Primavera, 1991;<br />
Hishamunda and Ridler, 2004). These <strong>systems</strong> have been proposed as a tool for<br />
develop<strong>in</strong>g environmentally sounded <strong>aquaculture</strong> practices and resource<br />
management with<strong>in</strong> a balanced coastal ecosystem approach (Troell et al., 2003;<br />
Neori et al., 2004). The polyculture of aquatic animals and plants reduces the<br />
environmental impact of the culture system compared to monoculture because of<br />
the reutilization of dissolved and particulate waste products (Petrell et al., 1993).<br />
Seaweed can absorb significant amounts of waste <strong>nutrient</strong>s, controll<strong>in</strong>g<br />
eutrophication, and consequently, improv<strong>in</strong>g the health and stability of mar<strong>in</strong>e<br />
eco<strong>systems</strong> (Buschmann et al., 2001; Chop<strong>in</strong> et al., 2001; Troell et al., 2003; Fei,<br />
2004; Neori et al., 2004). The physiological mechanisms of seaweed biofiltration<br />
have been studied <strong>in</strong>, e.g. filter-feed<strong>in</strong>g bivalve culture <strong>systems</strong> (Fang et al.,<br />
1996), fish cage farms (Troell et al., 1997; Hayashi et al., 2008), shrimp culture<br />
ponds (Jones et al., 2001; Nelson et al., 2001), and polyculture ponds conta<strong>in</strong><strong>in</strong>g<br />
shrimp Penaeus vannamei and seaweed Gracillaria verrucosa (Ihsan et al.,<br />
submitted).<br />
In an <strong>aquaculture</strong> system most of the nitrogenous and phosphorus dissolved<br />
<strong>in</strong>organic waste products are excreted <strong>in</strong> the form of ammonium (NH4 + ) and<br />
phosphate (PO4 3- ). Both compounds are potentially toxic to aquatic organisms and<br />
76
<strong>in</strong>crease eutrophication potential. The mechanical and chemical treatment and<br />
other processes to remove the excess of ammonium and phosphate from waste<br />
water and the culture ponds are very expensive and may also affect the<br />
environment (Troell et al., 2003). Seaweed has been studied <strong>in</strong> recent years for<br />
<strong>nutrient</strong> removal strategies. This treatment technique is considered to be the most<br />
<strong>in</strong>expensive and environmentally sounded clearification way (Buschmann et al.,<br />
1996; Rathakrishnan, 2001; Neori et al., 2004).<br />
The subject of the present study is the parameterization of the rate of nitrogen<br />
uptake by the seaweed from shrimp wastewater of polyculture <strong>systems</strong> <strong>in</strong> order to<br />
reduce the <strong>nutrient</strong> releases <strong>in</strong>to the environment.<br />
Material and Method<br />
The experiment was conducted <strong>in</strong> Sungai Buntu, West Java over a 40-day period<br />
from August–September 2009 <strong>in</strong> an <strong>in</strong>door laboratory facility (Figure 1). This<br />
study used a completely randomized block design conducted <strong>in</strong> two phases. Phase<br />
I aimed to determ<strong>in</strong>e optimal stock<strong>in</strong>g densities and ammonia excretion rates of<br />
shrimps, whereas the second phase quantified the nitrogen assimilation of<br />
seaweed at four seaweed stock<strong>in</strong>g densities.<br />
Location of experiments<br />
(Sungai Buntu-West Java)<br />
Figure 1. Map of Research <strong>Institut</strong>e for Brackish water fisheries, West Java,<br />
Indonesia<br />
77
The experiment <strong>in</strong> phase I was divided <strong>in</strong>to 3 treatments us<strong>in</strong>g glass aquaria with<br />
shrimp stock<strong>in</strong>g densities of 5, 10, and 15 <strong>in</strong>d/100 liters of water. For each<br />
treatment two replications were conducted. Phase I was carried out for 1 week.<br />
The aquarium was filled with 100 liters of aerated sea water, and the environment<br />
was controlled with temperatures <strong>in</strong> the range of 27–30 ° C and sal<strong>in</strong>ity rang<strong>in</strong>g<br />
from 25 to 28 ppt. Shrimp were fasted for one day then weighed; afterwards they<br />
were fed for one week and weighed aga<strong>in</strong> at the end of the experiment. On the last<br />
day, shrimp were transferred <strong>in</strong>to two conta<strong>in</strong>ers (10 liters), which had been filled<br />
with aerated sea water and exposed for 8 hours to ultraviolet (UV) light for<br />
dis<strong>in</strong>fection of other nitrogen-consum<strong>in</strong>g organisms. Stock<strong>in</strong>g density <strong>in</strong> the<br />
conta<strong>in</strong>ers was one shrimp per 5 liters. Two conta<strong>in</strong>ers without shrimp served as a<br />
control. Sampl<strong>in</strong>g was carried out 6 times at 1 h <strong>in</strong>tervals from 0–5 h. Afterwards<br />
ammonium nitrogen was measured <strong>in</strong> accordance to APHA standard methods<br />
(1995).<br />
In phase 2, nitrogen assimilation of seaweed at four stock<strong>in</strong>g densities of seaweed<br />
was <strong>in</strong>vestigated with 3 replications us<strong>in</strong>g concrete tanks (3 m³ volume, 1 m * 3 m<br />
* 1 m). Seaweed stock<strong>in</strong>g densities were 0 g/l (Treatment A), 3.125 g/l (Treatment<br />
B), 6.250 g/l (Treatment C), and 9.375 g/l of seaweed (Treatment D).<br />
Determ<strong>in</strong>ation of seaweed density was modified from Rathakrishnan (2001).<br />
Shrimp stock<strong>in</strong>g density used <strong>in</strong> experimental phase 2 amounted 5 shrimp/100<br />
liter with an <strong>in</strong>itial weight of 6–7 g, based on the outcome of growth and survival<br />
results of phase 1 experiments. Individual and total weight of the replicate tank<br />
load<strong>in</strong>g groups was not significantly different (P>0.05).<br />
The shrimp were fed a commercial diet with a prote<strong>in</strong> content of 40% four times a<br />
day, i.e. at 07.00, 12.00, 17.00 and 22.00. The feed quantity was dynamically<br />
assigned to shrimp biomass <strong>in</strong>crease estimated from control sampl<strong>in</strong>g. The daily<br />
feed ratio provided 7% of the weight of shrimp at sampl<strong>in</strong>g, modified <strong>in</strong><br />
accordance with Baliao and Tookw<strong>in</strong>as (2002). Subsamples of shrimps (number<br />
of <strong>in</strong>dividuals) and algae from each tank were weighed every week.<br />
78
Sampl<strong>in</strong>g<br />
In both phases of the experiment, the follow<strong>in</strong>g water quality parameters were<br />
measured: temperature, sal<strong>in</strong>ity, dissolved oxygen (DO), pH, ammonium, nitrate,<br />
nitrite, and total nitrogen (TN). Additionally, the number and weight of shrimp<br />
and survival rate, growth rate and feed conversion ratio (FCR) were assessed.<br />
In phase 2, every week, ammonium, nitrate, nitrite, and total nitrogen were<br />
analyzed. The samples were taken over a 24-hour period at 3 hour <strong>in</strong>tervals. Water<br />
samples were taken from 20 cm below the water surface. Everyday at 08.00 and<br />
16.00, the water temperature, sal<strong>in</strong>ity, and dissolved oxygen (DO) were monitored<br />
<strong>in</strong> situ with a portable water-quality analyser (TOA model WQC-20A Electronics<br />
Ltd., Japan). Water samples were collected us<strong>in</strong>g plastic bottles attached to the<br />
end of a stick. They were immediately filtered through Whatman GF/F filters 0.7<br />
µM millipore for soluble <strong>nutrient</strong>s analyses (NO3 - , NO2 - , NH4 + ). The ammonium<br />
concentration <strong>in</strong> the filtrate was measured immediately follow<strong>in</strong>g filtration. Total<br />
nitrogen (TN), nitrate, and nitrite concentrations were measured us<strong>in</strong>g the APHA<br />
(1995) standard method. The standard methods for the determ<strong>in</strong>ation of<br />
ammonium, nitrite and nitrate were based on moderate alkal<strong>in</strong>e solution with<br />
hypochlorite, diazotization, and cadmium reduction followed by diazotization,<br />
respectively. The spectrophotometer wave lengths for ammonium, nitrite, and<br />
nitrate were 630 nm, 542 nm, and 542 nm, respectively. The <strong>nutrient</strong> analyses<br />
were performed us<strong>in</strong>g a spectrophotometer (Shimadzu UV-2400).<br />
The nitrogen content <strong>in</strong> the feed, shrimp, and seaweed was measured us<strong>in</strong>g the<br />
Kjeldahl method. Subsamples of shrimp (quantity) and algae (quantity) were<br />
analyzed at the beg<strong>in</strong>n<strong>in</strong>g and the end of the experiment to assess changes <strong>in</strong><br />
nitrogenous composition.<br />
Calculation<br />
Survival Rate (SR) was calculated as a ratio of the shrimps quantity at stock<strong>in</strong>g<br />
and sampl<strong>in</strong>g time us<strong>in</strong>g the follow<strong>in</strong>g formula:<br />
SR = (Nt / N0) X 100%<br />
With: SR = survival rate<br />
79
N 0 = number of shrimp on day 0 (<strong>in</strong>dividuals)<br />
Nt = number of shrimp on day t (<strong>in</strong>dividuals)<br />
Specific growth rate were calculated with the formula (Busacker et al., 1990):<br />
SGR = ((ln Wt - ln W0) / t) * 100%<br />
With: SGR = Specific growth rate<br />
W 0 = weight on day-0 (g/<strong>in</strong>dividual)<br />
Wt = weight on day-t (g/<strong>in</strong>dividual)<br />
t = time of experiment (day)<br />
The feed conversion ratio (FCR) was calculated as the ratio between the amount<br />
of feed given to shrimp biomass <strong>in</strong>crement at a certa<strong>in</strong> period (NRC, 1977) us<strong>in</strong>g<br />
the formula:<br />
FCR = F / ΔB<br />
With: FCR = feed conversion ratio<br />
F = amount of feed given dur<strong>in</strong>g experiment (kg)<br />
ΔB = addition of shrimp biomass dur<strong>in</strong>g experiment (kg)<br />
Nitrogen retention was calculated based on the follow<strong>in</strong>g equation:<br />
NR = ∑TNt - ∑TN0<br />
With: NR = Nitrogen retention (g)<br />
∑TNt = amount of total nitrogen on day-t (g)<br />
∑TN0 = amount of total nitrogen on day-0 (g)<br />
Ammonium excretion was calculated based on the follow<strong>in</strong>g equation (Yigid,<br />
2005):<br />
AE = ((Nt – N0)/(W * Tt-0))<br />
With: AE = Ammonium excretion (mg-N/g/h)<br />
Nt = Ammonium concentration on time-t (mg/l)<br />
N0 = Ammonium concentration on time-0 (mg/l)<br />
W = weight of shrimp (g)<br />
Tt-0= sampl<strong>in</strong>g <strong>in</strong>terval<br />
80
Statistics<br />
Growth rate, survival rate, nitrogen retention and <strong>nutrient</strong> <strong>fluxes</strong> from experiments<br />
were analyzed statistically. All data were checked for normality (Kolmogorov-<br />
Smirnov test) and homogeneity of variances (HOV, Brown Forsythe test).<br />
Differences of means of triplicates <strong>in</strong> phase 2 were evaluated for significance by<br />
the range tests of Tukey HSD (P
ammonium excretion was 0.004 mg/g/h. The results of the first phase ammonia<br />
excretion trial are summarized <strong>in</strong> Table 2.<br />
Table 2. Ammonium Excretion<br />
Conta<strong>in</strong>ers<br />
Time observation (h)<br />
0 1 2 3 4 5<br />
Weight<br />
of<br />
shrimp<br />
(g)<br />
Ammonium<br />
excretion<br />
(mg/g/h)<br />
Replicate1 0.356 0.438 0.535 0.603 0.671 0.620 7.89 0.005<br />
Replicate2 0.544 0.586 0.540 0.580 0.660 0.643 8.21 0.003<br />
Average 0.450 0.512 0.537 0.591 0.665 0.631 8.05 0.004<br />
Phase II<br />
Growth of shrimp<br />
The total weight of shrimp at the end of the experiment was significantly different<br />
between treatments (P0.05) among the treatment without seaweed<br />
and the treatment with stock<strong>in</strong>g of seaweed 3.125 g/l (B), 6.250 g/l (C), and 9.375<br />
g/l (D) (Figure 2).<br />
The survival rate (SR) of shrimp <strong>in</strong> phase II, showed that from the first week until<br />
the end of the study there was a significant difference (P
Table 3. Weight, Retention, and FCR<br />
Treatment<br />
A B C D<br />
Total N-Feed (g) 16.44 18.09 16.9 18.41<br />
Start<br />
Weight shrimp (g) 266.41 265.95 269.74 266.81<br />
N shrimp (%) 7.44 7.43 7.53 7.45<br />
Weight Seaweed (g) 1562.6 3125.26 4688.29<br />
N Seaweed (%) 8.06 16.13 24.19<br />
End<br />
Weight shrimp (g) 243.78 a<br />
N shrimp (%) 1.78 a<br />
350.2 b<br />
10.16 b<br />
327.96 c<br />
9.13 b<br />
Weight Seaweed (g) 3255.12 a 5963.78 b<br />
N Seaweed (%) 22.68 a<br />
N-Retention<br />
Shrimp (g) 0.59 a<br />
2.73 b<br />
Seaweed (g) 14.62 a<br />
N production of shrimp 15.85 a<br />
N <strong>in</strong> water (g) 15.85 a<br />
FCR 2.69 a<br />
15.36 a<br />
0.74 b<br />
1.99 a<br />
Daily Growth rate of<br />
Seaweed (%) 2.62 a<br />
24.67 a<br />
1.6 c<br />
8.54 b<br />
15.3 a<br />
6.76 c<br />
2.02 a<br />
2.31 a<br />
314.71 d<br />
9.22 b<br />
6563.24 b<br />
36.65 b<br />
1.78 c<br />
12.46 c<br />
16.63 a<br />
4.18 c<br />
2.24 a<br />
1.20 b<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
83
Weight (g)<br />
18.00<br />
17.00<br />
16.00<br />
15.00<br />
14.00<br />
13.00<br />
12.00<br />
11.00<br />
10.00<br />
a<br />
a<br />
Weight Average of Shrimp<br />
a<br />
a<br />
0 1 2 3 4 5<br />
Time (Week)<br />
a<br />
a<br />
a<br />
a<br />
Seaweed 0 g/l<br />
Seaweed 3.125 g/l<br />
Seaweed 6.250 g/l<br />
Seaweed 9.375 g/l<br />
Figure 2. Individual weight of shrimp dur<strong>in</strong>g the experimental period, values<br />
Survival rate (% )<br />
are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
120.00<br />
100.00<br />
80.00<br />
60.00<br />
40.00<br />
20.00<br />
0.00<br />
b b<br />
a a<br />
Survival Rate<br />
0 1 2 3 4 5<br />
b<br />
a<br />
Time (Week)<br />
b<br />
a<br />
b<br />
b<br />
Seaweed 0 g/l<br />
Seaweed 3.125 g/l<br />
Seaweed 6.250 g/l<br />
Seaweed 9.375 g/l<br />
Figure 3. Survival Rate of shrimp dur<strong>in</strong>g the experimental period, values are<br />
mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
84
Growth of seaweed<br />
The daily growth rate of seaweed was significantly different (P0.05).<br />
The lowest FCR value occurred <strong>in</strong> the treatment with stock<strong>in</strong>g density of seaweed<br />
3.125 g/l (treatment B) i.e. 1.99 and the highest occurred <strong>in</strong> the treatment without<br />
seaweed (treatment A) i.e. 2.69.<br />
Nitrogen retention of shrimp <strong>in</strong> each treatment was significantly different<br />
(P
Concentration (m g/l)<br />
Concentration (m g/l)<br />
3.5<br />
3<br />
2.5<br />
2<br />
1.5<br />
1<br />
0.5<br />
0<br />
a<br />
b<br />
a<br />
b<br />
Total Nitrogen<br />
0 1 2 3 4 5<br />
a<br />
Time (Week)<br />
b<br />
a<br />
b<br />
b<br />
b<br />
Seaweed 0 g/l<br />
Seaweed 3.125 g/l<br />
Seaweed 6.250 g/l<br />
Seaweed 9.375 g/l<br />
Figure 4. Concentration of total nitrogen (TN) dur<strong>in</strong>g the experimental<br />
1.2<br />
1<br />
0.8<br />
0.6<br />
0.4<br />
0.2<br />
0<br />
period, values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
a<br />
b<br />
b<br />
b<br />
b<br />
b<br />
c<br />
a<br />
Ammonium<br />
0 1 2 3 4 5<br />
d<br />
c<br />
b<br />
Time (Week)<br />
a<br />
c<br />
a<br />
b<br />
Seaweed 0 g/l<br />
Seaweed 3.125 g/l<br />
Seaweed 6.250 g/l<br />
Seaweed 9.375 g/l<br />
Figure 5. Concentration of ammonium-nitrogen (NH4 - -N) dur<strong>in</strong>g the<br />
experimental period, values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
86
Even though fresh water was supplied to the ponds, the ammonium-nitrogen<br />
concentrations occurred <strong>in</strong> different amounts <strong>in</strong> all treatments. The highest<br />
concentration of ammonium occurred <strong>in</strong> treatment A (without seaweed) at week 2,<br />
i.e. 0.94 mg/l (Figure 5).<br />
Nitrate showed a different pattern as well. The peak nitrate concentration <strong>in</strong> all<br />
treatments was 0.009 mg/l. Treatment (A) occurred at week 1, treatment (B) at<br />
week 2, treatment (C) at week 4, and treatment (D) at week 3 (Figure 6). While<br />
nitrite showed the same pattern <strong>in</strong> all treatments. The peak concentration of nitrite<br />
<strong>in</strong> all treatments occurred at week 2 and not significantly different (P>0.05).<br />
Treatment (A) was 0.009 mg/l, treatment (B) 0.007 mg/l, treatment (C) 0.008<br />
mg/l, and treatment (D) 0.009 mg/l (Figure 7).<br />
Concentration (mg/l)<br />
0.012<br />
0.01<br />
0.008<br />
0.006<br />
0.004<br />
0.002<br />
0<br />
a<br />
a<br />
b<br />
b<br />
c<br />
a<br />
Nitrate<br />
0 1 2 3 4 5<br />
b<br />
c<br />
Time (WeeK)<br />
Seaweed 0 g/l<br />
Figure 6. Concentration of Nitrate-nitrogen (NO3 - -N) dur<strong>in</strong>g the<br />
experimental period, values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
87<br />
a<br />
a<br />
c<br />
b<br />
Seaweed 3.125 g/l<br />
Seaweed 6.250 g/l<br />
Seaweed 9.375 g/l
Concentration (m g/l)<br />
0.01<br />
0.009<br />
0.008<br />
0.007<br />
0.006<br />
0.005<br />
0.004<br />
0.003<br />
0.002<br />
0.001<br />
0<br />
a<br />
a<br />
a<br />
a<br />
a<br />
a<br />
Nitrite<br />
0 1 2 3 4 5<br />
a<br />
Time (Week)<br />
a<br />
a<br />
a<br />
a<br />
a<br />
Seaweed 0 g/l<br />
Seaweed 3.125 g/l<br />
Seaweed 6.250 g/l<br />
Seaweed 9.375 g/l<br />
Figure 7. Concentration of Nitrite-nitrogen (NO2 - -N) dur<strong>in</strong>g the experimental<br />
period, values are mean of triplicate ponds (n=3)<br />
Values with the same superscript letter do not differ significantly (P>0.05)<br />
Discussion<br />
Utilization of dissolved nitrogen by seaweed <strong>in</strong> the water aims to reduce the waste<br />
burden <strong>in</strong> the <strong>aquaculture</strong> media. Nitrogen content of the treatment us<strong>in</strong>g the<br />
seaweed was <strong>in</strong>creased but it did not get too high (Figure 4), prov<strong>in</strong>g that the<br />
seaweed Gracillaria verrucosa could take up nitrogen. The seaweed could make<br />
use of ammonium through a diffusion process us<strong>in</strong>g all parts of its body. The<br />
higher the ability of seaweed to absorb the dissolved ammonium, the greater its<br />
growth. This means that the content of nitrogen will also further <strong>in</strong>crease <strong>in</strong> the<br />
seaweed biomass, which can be seen from nitrogen seaweed bladder <strong>in</strong>creases.<br />
Nitrogen is necessary for the seaweed <strong>in</strong> the regulation of metabolism and<br />
reproduction. Growth and biomass can be achieved properly if the seaweed<br />
receives sufficient nitrogen. Uptake of nitrogen by seaweed Gracillaria verrucosa<br />
is not only a function of external nitrogen concentration, but also of the <strong>in</strong>ternal<br />
concentration <strong>in</strong> the plant net. Retrieval and storage of nitrogen by the seaweed<br />
can be affected by the concentration of dissolved <strong>in</strong>organic nitrogen <strong>in</strong> water and<br />
88
<strong>in</strong>fluenced by ecological fluctuations of nitrogen <strong>in</strong> plant tissues. Low nitrogen<br />
concentrations <strong>in</strong> the environment cannot meet the needs of seaweed for nitrogen<br />
for further usage. But the seaweed has the ability to assimilate and store <strong>nutrient</strong>s<br />
from its surround<strong>in</strong>gs, especially at low concentrations. Nitrogen dry weight<br />
content <strong>in</strong> treatments C and D were lower than treatment B. Presumably, although<br />
the amount of nitrogen <strong>in</strong> the form of nitrate and nitrite <strong>in</strong> water is high but<br />
Gracillaria was less able to utilize it. This is consistent with the f<strong>in</strong>d<strong>in</strong>g that the<br />
most nitrogen absorbed by the seaweed is nitrogen <strong>in</strong> ammonium form (Troell et<br />
al., 1999). To meet the need for nitrogen, the reserves stored <strong>in</strong> the network are<br />
used prior to growth.<br />
The ability of seaweed <strong>in</strong> tak<strong>in</strong>g up nitrogen from shrimp <strong>aquaculture</strong> waste <strong>in</strong><br />
different treatments dur<strong>in</strong>g the four weeks of ma<strong>in</strong>tenance <strong>in</strong> treatment B,<br />
seaweed was capable of utiliz<strong>in</strong>g dissolved nitrogen from shrimp waste up to<br />
14.62 g, so that the weight of seaweed would be <strong>in</strong>creas<strong>in</strong>g twice. If it was<br />
calculated per hour, then the seaweed is capable of absorb<strong>in</strong>g dissolved nitrogen<br />
at a rate of 0.013 g-N/kg/hr. The utilization of nitrogen by seaweed <strong>in</strong> this study is<br />
higher than the results of the previous study (Ihsan et al., submitted). In the<br />
previous study, the TN of seaweed <strong>in</strong> polyculture system was 3.5%. In phase 2 of<br />
the study, the absorption of nitrogen by seaweed was three times greater than the<br />
production value of nitrogen excretion of shrimp per hour and kilogram <strong>in</strong> study<br />
phase I (Table 1). This means that dissolved nitrogen excretion of the shrimp can<br />
be utilized optimally by the seaweed.<br />
Utilization of ammonium at treatments C (6.250 g/l of seaweed) and D (9.375 g/l<br />
of seaweed) is greater than for treatment B (3.125 g/l of seaweed) only at the<br />
beg<strong>in</strong>n<strong>in</strong>g of the study (first week). This condition does not last as long as the<br />
amount of ammonium reduced. To meet <strong>nutrient</strong> needs, seaweed then utilizes<br />
nitrate and nitrite. It can be seen from the steady depletion of nitrate and nitrite<br />
content <strong>in</strong> <strong>aquaculture</strong> media. In general, seaweed gradually absorbs nitrogen, i.e.<br />
ammonium> nitrate> nitrite (Troell et al., 1999). Utilization of nitrate and nitrite<br />
by the seaweed is less efficient because nitrate and nitrite must first be reduced<br />
before used by seaweed. Seaweed us<strong>in</strong>g nitrate for the metabolism need<br />
<strong>in</strong>volvement of nitrate reductase enzyme (Patadjai, 1993). Absorption of nitrate<br />
89
and nitrite by the seaweed is <strong>in</strong>fluenced by the concentration of ammonium <strong>in</strong> the<br />
media. Due to the nitrogen used by seaweed <strong>in</strong> treatments C and D be<strong>in</strong>g nitrate<br />
and nitrite, then the growth of seaweed was not as fast at the beg<strong>in</strong>n<strong>in</strong>g of more<br />
research utiliz<strong>in</strong>g ammonium. Soriano (2002) reported the growth of seaweed<br />
dur<strong>in</strong>g the first two weeks as rapid, but that it then decl<strong>in</strong>ed until the end.<br />
Ma<strong>in</strong>tenance of seaweed Gracillaria verrucosa <strong>in</strong> dra<strong>in</strong> ponds of shrimp <strong>in</strong> the<br />
first 15 days reached 8.8% and then cont<strong>in</strong>ued to decl<strong>in</strong>e.<br />
Glen et al. (2002) showed that seaweed Gracillaria parvispora cultivation <strong>in</strong><br />
shrimp pond effluent water could <strong>in</strong>crease the nitrogen content <strong>in</strong> the thallus of<br />
1% to 3.5% with a growth rate of 8–9% per day, which is higher than the growth<br />
rate of seaweed fed chemical fertilizers i.e. only 4–5% per day. The content of<br />
ammonium <strong>in</strong> treatment A (without seaweed) <strong>in</strong> the second week decreased<br />
drastically. This is due to the oxidation of ammonium <strong>in</strong>to nitrite and then <strong>in</strong>to<br />
nitrate. The content of nitrite and nitrate <strong>in</strong>creased until reach<strong>in</strong>g a peak; this is<br />
due to the aeration of the culture medium so that the oxygen demand for oxidation<br />
processes is met. Boyd (1999) described the process of oxidation with ammonium<br />
as the energy source, CO2 as a carbon source and O2 the source for the oxidation<br />
process. The oxidation process also occurred <strong>in</strong> treatments B, C, and D but <strong>in</strong><br />
small quantities because the ammonium first utilized by seaweed. Besides that,<br />
seaweed also produces oxygen from photosynthesis rest. Xu (2008) reported<br />
Gracillaria cultivation can improve other aspects of water quality <strong>in</strong>stead of<br />
<strong>in</strong>creas<strong>in</strong>g DO. Its photosynthesis produces DO, which promotes decomposition<br />
of organics. Density raft culture of Gracillaria verrucosa impedes the water<br />
circulation and may reduce chemical oxygen demand (COD) <strong>in</strong> the water column.<br />
In addition, several species of Gracillaria can produce oxygen under low light<br />
conditions, such as <strong>in</strong> ra<strong>in</strong>y days and remediate anoxia (Xu et al., 2004). Neori et<br />
al. (2004) reported that seaweed Gracillaria sp. is capable of supply<strong>in</strong>g oxygen<br />
(DO) of 2.86 mg/l for 24 hours to the ma<strong>in</strong>tenance medium us<strong>in</strong>g polyculture with<br />
milkfish, shrimp, and seaweed.<br />
Ammonium concentrations <strong>in</strong>creased aga<strong>in</strong> <strong>in</strong> all treatments dur<strong>in</strong>g week 4, with<br />
the highest value <strong>in</strong> treatment (D). This is due to the feed<strong>in</strong>g; the higher residual<br />
and fecal excretion issued shrimp and dead seaweed. Additionally the maximum<br />
90
growth of seaweed was achieved <strong>in</strong> the third week. When maximum growth has<br />
been achieved then the absorption of nitrogen will decrease.<br />
Water quality greatly affects the growth of shrimp. Good water quality is capable<br />
of support<strong>in</strong>g shrimp life, thereby <strong>in</strong>creas<strong>in</strong>g the appetite of the shrimp. Based on<br />
the value of FCR and the retention of each treatment, it is known that the FCR<br />
<strong>in</strong>dicates the efficiency level of the feed utilization by shrimp as well as affect<strong>in</strong>g<br />
the <strong>nutrient</strong> waste load discharged <strong>in</strong>to the environment. The smallest FCR<br />
occurred <strong>in</strong> treatment B (1.99) with a biomass of 350.2 g and survival rate of<br />
82.67%. This means that the high feed utilization by shrimp for growth causes the<br />
retention value also to be high (2.73 g). In comparison to the global average<br />
shrimp feed conversion ratio of around 2.0, the observed feed conversion were<br />
quite good (Tacon, 2002).<br />
The concentration of ammonium and nitrite <strong>in</strong> treatment (B) was lower compared<br />
with other treatments. To grow the shrimp from 265.95 g to 350.16 g, 15.36 g of<br />
nitrogen waste were generated (Table 3). Most of the waste (14.62 g) was<br />
absorbed by the seaweed, which enabled it to grow to1.69 kg, while the rema<strong>in</strong><strong>in</strong>g<br />
0.74 g of residual waste rema<strong>in</strong>ed <strong>in</strong> the water. The smaller the concentration of<br />
nitrogen rema<strong>in</strong><strong>in</strong>g <strong>in</strong> the water, the more effective the utilization rate of nitrogen<br />
by the seaweed.<br />
Conclusions<br />
The seaweed Gracillaria verrucosa can be cultivated <strong>in</strong> polyculture together with<br />
the shrimp Penaeus vannamei. The ability of seaweed <strong>in</strong> tak<strong>in</strong>g up nitrogen from<br />
the water would make the farm<strong>in</strong>g environment better and support shrimp<br />
production. This can be seen from the survival rates (SR) be<strong>in</strong>g significantly<br />
different (P
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Naylor, R. L., R. J. Goldburg, J.H. Primavera, N. Kautsky, M. C. Beveridge, J<br />
Clay, C. Folke, J. Lubchenco, H Mooney, M Troell. 2000. Effect of<br />
<strong>aquaculture</strong> on world fish supplies. Nature 405:1017–1024.<br />
Nelson, S. G., E. P. Glenn, J. Conn, D. Moore D, T. Walsh, M. Akutagawa. 2001.<br />
Cultivation of Gracillaria parvispora (Rhodophyta) <strong>in</strong> shrimp-farm<br />
effluent ditches and float<strong>in</strong>g cages <strong>in</strong> Hawaii: a two phase polyculture<br />
system. Aquaculture 193:239–248.<br />
Neori, A., T. Chop<strong>in</strong> T, M. Troell, A. H. Buschmann, G.P. Kraemer, C. Hall<strong>in</strong>g,<br />
M. Shpigel, C Yarish. 2004. Integrated <strong>aquaculture</strong>: rationale, evolution<br />
and state of the art emphasiz<strong>in</strong>g seaweed biofiltration <strong>in</strong> modern<br />
mariculture. Aquaculture 231:361–391.<br />
Petrell, R. J., T. K. Mazhari, P.J. Harrison, L. D. Druehl. 1993. Mathematical<br />
model of Lam<strong>in</strong>aria production near a British Columbian salmon sea cage<br />
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Porter, C.B., M.D. Krom, M.G. Rob<strong>in</strong>ns, L. Brickell, A. Davidson. 1987.<br />
Ammonia excretion and total nitrogen budget for Gilthead sea bream<br />
(Sparu aurata) and its effects on water quality conditions. Aquaculture,<br />
66: 287-297. Curr. Res. J. Biol. Sci., 2(2): 150-153, 2010.<br />
Primavera, J. 1991. Intensive prawn farm<strong>in</strong>g <strong>in</strong> the Philipp<strong>in</strong>es: ecological, social,<br />
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Rathakrishnan. 2001. Removal of nitrogenous wastes by seaweeds <strong>in</strong> closed<br />
Lobster culture <strong>systems</strong>. J. M ar. Biol. Ass. Ind., 43(1,2): 181-185.<br />
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Ruddle, K., G. F. Zong. 1988. Integrated agriculture–<strong>aquaculture</strong> <strong>in</strong> South Ch<strong>in</strong>a.<br />
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effluents <strong>in</strong> constructed wetland with emergent plants and subsurface<br />
horizontal water flow. Aquaculture. Elsevier. 217: 207-221.<br />
Shpigel, M., A. Neori. 1996. The <strong>in</strong>tegrated culture of seaweed, abalone, fish and<br />
clams <strong>in</strong> modular <strong>in</strong>tensive land-based <strong>systems</strong>: J Appl Phycol (2009)<br />
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shrimp <strong>aquaculture</strong>. Report prepared under the World Bank, NACA,<br />
WWF and FAO consortium program on shrimp farm<strong>in</strong>g and the<br />
environment, published by consortium, 69.<br />
Troell, M., C. Hall<strong>in</strong>g, A Nilsson, A. H. Buschmann., N. Kautsky, L. Kautsky.<br />
1997. Integrated mar<strong>in</strong>e cultivation of Gracillaria chilensis (Gracilariales,<br />
Bangiophyceae) and salmon cages for reduced environmental impact and<br />
<strong>in</strong>creased economic output. Aquaculture 156:45–61.<br />
Troell, M., P. Ronnback, C. Hall<strong>in</strong>g, N. Kautsky and A.H. Buschmann. 1999.<br />
Ecological eng<strong>in</strong>eer<strong>in</strong>g <strong>in</strong> <strong>aquaculture</strong>: Use of seaweeds for remov<strong>in</strong>g the<br />
<strong>nutrient</strong>s from the <strong>in</strong>tensive mariculture. J. Appl. Phycol., 11: 89-97.<br />
Troell M, C. Hall<strong>in</strong>g, A. Neori, T. Chop<strong>in</strong>, A. H. Buschmann, N. Kautsky, C.<br />
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94
General Discussion<br />
System performance<br />
In recent years, polyculture system has been proposed as a key to develop<br />
environmentally sounded <strong>aquaculture</strong> practices and resource management through<br />
a balanced ecosystem approach to avoid pronounced shifts <strong>in</strong> coastal areas. Feed<br />
based <strong>aquaculture</strong> needs to be <strong>in</strong>tegrated with extractive <strong>aquaculture</strong>. Multitrophic<br />
polyculture system provides bioremediation potential, mutual benefits to the cocultured<br />
organism, economic diversification by creat<strong>in</strong>g other value added<br />
products and <strong>in</strong>crease profitability per cultivation unit.<br />
In chapter one, based on a literature study polyculture system are described as the<br />
practice of cultur<strong>in</strong>g more than one species of aquatic organism <strong>in</strong> the same<br />
system. The motivat<strong>in</strong>g pr<strong>in</strong>ciple is that fish/shrimp production may be<br />
maximized by rais<strong>in</strong>g a comb<strong>in</strong>ation of species hav<strong>in</strong>g different food habits. The<br />
concept of polyculture of fish/shrimp is based on the concept of total utilization of<br />
different trophic and spatial niches of a pond <strong>in</strong> order to obta<strong>in</strong> maximum<br />
fish/shrimp production per unit area (Edward, 1992; Chiang, 1993; Qian et al.,<br />
1996). The ma<strong>in</strong> advantages of polyculture <strong>systems</strong> is that wastes of one resource<br />
user become a source for the others (Neori et al., 2004).<br />
The use of seaweed <strong>in</strong>tegrated with fish/shrimp cultures has been studied <strong>in</strong> open<br />
water and land-based system condition <strong>in</strong> Israel, Portugal, Brazil, and Indonesia<br />
(Neori et al., 1998; Schuenhoff et al., 2003; Lombardi et al., 2006; Ihsan et al.,<br />
submitted). General concepts about <strong>nutrient</strong> uptake by seaweed can be found <strong>in</strong><br />
Harrison and Hurd (2001). To optimize the seaweed component of an <strong>in</strong>tegrated<br />
<strong>aquaculture</strong> system, particular attention should be given not only to physical and<br />
chemical factors such as light, temperature, effluent <strong>nutrient</strong> concentration and<br />
flux, and water motion but also to biological factors such as plant variability<br />
<strong>in</strong>clud<strong>in</strong>g tissue type, plant age, etc.<br />
Xu (2008) reported the Gracillaria cultivation can improve other aspect of water<br />
quality <strong>in</strong>stead of <strong>in</strong>creas<strong>in</strong>g DO. Its photosynthesis produces DO that promotes<br />
decomposition of organics. Density raft culture of Gracillaria impedes the water<br />
circulation and may decrease chemical oxygen demand (COD) <strong>in</strong> the water<br />
95
column. In addition, several species of Gracillaria can produce oxygen under low<br />
light condition, such as <strong>in</strong> ra<strong>in</strong>y days and remediate anoxia (Xu et al., 2004).<br />
In chapter two, polyculture <strong>systems</strong> us<strong>in</strong>g seaweed Gracillaria seem to act more<br />
efficiently with regard to <strong>nutrient</strong> accumulation than <strong>in</strong> monoculture. The average<br />
ammonium-nitrogen concentration over the whole period was 0.24 mg/l <strong>in</strong><br />
polyculture while <strong>in</strong> monoculture 0.37 mg/l of ammonium-nitrogen were<br />
analyzed. Survival rate of shrimp <strong>in</strong> polyculture and monoculture were 86.32%<br />
and 69.17%, respectively.<br />
Growth performance<br />
Overall, the growth performance of shrimp <strong>in</strong> polyculture was better than<br />
monoculture <strong>systems</strong>. In chapter two, the average f<strong>in</strong>al weight of shrimp was 24.9<br />
± 1.8 g for polyculture <strong>systems</strong> with survival rates of 86.3%. For monoculture, the<br />
weight of shrimp was 20.8 ± 1.05 g and survival rate accounted 69.17%. Survival<br />
rate of shrimp <strong>in</strong> polyculture was significantly higher than <strong>in</strong> monoculture, and the<br />
weight of shrimp as well. The feed conversion ratio (FCR) for the polyculture and<br />
monoculture system <strong>in</strong> this study were significantly (P0.05). The average weight of shrimp at harvest was 24.73<br />
± 0.71 and 23.45 ± 1.43 g/<strong>in</strong>d for polyculture I and II, respectively. Specific<br />
growth rate (SGR) for shrimp <strong>in</strong> polyculture I and II was not significantly<br />
different (P>0.05) with an average value over the 90-day experiment of 4.5%/day<br />
and 4.4%/day, respectively.<br />
Shrimp growth and production were reported to be basically related to the<br />
environmental condition (Songsangj<strong>in</strong>da, 1994). Results from this study showed<br />
clear differences <strong>in</strong> performance parameters between monoculture and polyculture<br />
<strong>systems</strong>. This result may <strong>in</strong>dicate that seaweed play a vital role on system<br />
productivity. This result is <strong>in</strong> agreement with the observation of Troell et al.<br />
(1997) and Soriano et al. (2002). They reported that the environmental conditions<br />
for growth of shrimp <strong>in</strong> polyculture <strong>systems</strong> is better than <strong>in</strong> monoculture. Apart<br />
96
from remov<strong>in</strong>g <strong>nutrient</strong>s, the seaweed as co-cultured organisms may contribute to<br />
the oxygen budget of the ponds.<br />
Fluctuation of water quality <strong>in</strong> ponds is the result of variation <strong>in</strong> <strong>nutrient</strong>s load<strong>in</strong>g<br />
from feed and biological processes of shrimp and organisms <strong>in</strong> water column<br />
(Burford and Williams, 2001).<br />
In chapter three, the water quality <strong>in</strong> polyculture <strong>systems</strong> were <strong>in</strong> optimal ranges<br />
for fish and shrimp <strong>in</strong>dicated by a high survival rate (SR) dur<strong>in</strong>g the 90-day<br />
period. Results from this study showed, that no significant differences <strong>in</strong> shrimp<br />
performance between the two polyculture <strong>systems</strong>. Shrimp growth and production<br />
correlated with stock<strong>in</strong>g density, feed<strong>in</strong>g management and water quality. The<br />
ma<strong>in</strong> <strong>nutrient</strong>s were <strong>in</strong>troduced <strong>in</strong>to the ponds via feed application. This suggests<br />
that pellet feed may properly promote <strong>nutrient</strong> excretion by shrimp and fish that<br />
can cause hypoxic conditions due to decomposition of organic material by<br />
bacteria <strong>in</strong> the bottom layer of the pond.<br />
Nutrient flux<br />
The two significant components of the pond environment are the pond water and<br />
sediment which <strong>in</strong>teract cont<strong>in</strong>uously to <strong>in</strong>fluence the culture environment. Pond<br />
sediment can be further divided <strong>in</strong>to the pond soil component (the pond bottom<br />
and walls) and the accumulated sediment component (Briggs and Funge-Smith,<br />
1994). In the <strong>in</strong>vestigation by Funge-Smith and Briggs (1998), around 90% of<br />
nitrogen <strong>in</strong>put to the pond came from feed but most of the nitrogen (70-80%) was<br />
not reta<strong>in</strong>ed <strong>in</strong> shrimp body, but rema<strong>in</strong> <strong>in</strong> the pond as accumulated sediment.<br />
In chapter two, the ammonium concentration <strong>in</strong>creased gradually <strong>in</strong> monoculture<br />
and polyculture <strong>systems</strong> and orthophosphate concentration progressively<br />
<strong>in</strong>creased as well. Though well water was supplied to the pond, the ammoniumnitrogen<br />
concentrations <strong>in</strong> monoculture <strong>in</strong>creased from 0.005 to 0.779 mg/l, with<br />
an average concentration of ammonium-nitrogen dur<strong>in</strong>g the 100 days period of<br />
0.37 mg/l. In polyculture system, it <strong>in</strong>creased from 0.003 to 0.483 mg/l, with an<br />
average of 0.24 mg/l. Therefore, ammonium-nitrogen concentrations <strong>in</strong><br />
monoculture system were significantly higher <strong>in</strong> comparison to polyculture<br />
system (P
Ideally, <strong>nutrient</strong> process <strong>in</strong> polyculture system with two or more ecologically<br />
compatible species should be balanced, waste from one species are recycled as<br />
fertilizer or feed by another without conflict<strong>in</strong>g with each other (Neori et al.,<br />
2000). By <strong>in</strong>tegrat<strong>in</strong>g fed mariculture (fish and shrimp) with extractive<br />
mariculture (seaweed), the wastes of one resource consumer become a source<br />
(fertilizer or feed) for others <strong>in</strong> the system. To get more <strong>in</strong>formation about<br />
optimum <strong>nutrient</strong> utilization, the absorbtion of nitrogen derived by shrimp waste<br />
<strong>in</strong>to seaweed Gracillaria verrucosa is described <strong>in</strong> chapter four.<br />
In chapter four, the total nitrogen (TN) concentration <strong>in</strong>creased gradually. It<br />
shows that the concentration of total nitrogen (TN) <strong>in</strong>creased <strong>in</strong> polyculture and<br />
monoculture system. The highest <strong>in</strong>crease of TN occurred <strong>in</strong> monoculture system<br />
(treatment without seaweed) from 0.82 to 2.73 mg/. The lowest <strong>in</strong>crease occurred<br />
<strong>in</strong> polyculture us<strong>in</strong>g seaweed at stock<strong>in</strong>g densities of 9.375 g/l (treatment D)<br />
rang<strong>in</strong>g from 0.55 to 1.46 mg/l.<br />
Mass balance<br />
In chapter two, a mass balance model was developed for total nitrogen and total<br />
phosphorus to estimate their <strong>fluxes</strong>. From the total nitrogen and total phosphorus<br />
<strong>in</strong>put, 24.2% and 5.3% were <strong>in</strong>corporated <strong>in</strong> 335.7 kg/1200 m 2 shrimp weight ga<strong>in</strong><br />
<strong>in</strong> monoculture, while 30.8% and 6.9% were <strong>in</strong>corporated <strong>in</strong> 501.5 kg/1200m 2<br />
shrimp weight ga<strong>in</strong> and 3.5% and 2.4% were <strong>in</strong>corporated <strong>in</strong> 325 kg/1200 m 2<br />
seaweed Gracillaria <strong>in</strong> polyculture system.<br />
In chapter three, mass balance model <strong>in</strong> this study showed <strong>nutrient</strong> utilization <strong>in</strong><br />
the evaluated polyculture <strong>systems</strong>. TN and TP <strong>in</strong>corporated <strong>in</strong> shrimp and<br />
seaweed <strong>in</strong> polyculture I was lower than polyculture <strong>systems</strong> II but not significant<br />
different.<br />
Conclusion<br />
Responsible <strong>aquaculture</strong> practices should be based on a balanced ecosystem<br />
management approach, which <strong>in</strong>corporate the biological and environmental<br />
function of a diverse group of organisms <strong>in</strong>to a unified system that ma<strong>in</strong>ta<strong>in</strong>s the<br />
natural <strong>in</strong>teraction of species and allows an ecosystem to function susta<strong>in</strong>able. In<br />
98
general, shrimp and fish <strong>aquaculture</strong> us<strong>in</strong>g additional feed produces a large<br />
amount of waste, <strong>in</strong>clud<strong>in</strong>g nitrogen and phosphorus that could be released <strong>in</strong>to<br />
the aquatic environment if not treated.<br />
Integrated seaweed <strong>aquaculture</strong> <strong>systems</strong> have been suggested as a possible<br />
solution for secur<strong>in</strong>g an <strong>in</strong>creas<strong>in</strong>g and environmentally sounded production of<br />
future supply.<br />
Normally, production of ma<strong>in</strong> target organism <strong>in</strong> polyculture system could<br />
decrease due to competition <strong>in</strong> space and <strong>nutrient</strong> utilization with co-cultured<br />
organisms. The results <strong>in</strong> this study suggest that seaweed can not only serve as an<br />
effective biofilter for shrimp ponds but also can <strong>in</strong>crease shrimp production even<br />
<strong>in</strong>tegrated with fish with<strong>in</strong> the same system. The weight and survival rate of<br />
shrimp <strong>in</strong> polyculture <strong>systems</strong> were higher than <strong>in</strong> monoculture.<br />
The ability of seaweed <strong>in</strong> tak<strong>in</strong>g up nitrogen from the water would make the<br />
farm<strong>in</strong>g environment better and support shrimp production. Thus polyculture<br />
<strong>systems</strong> us<strong>in</strong>g seaweed seem to act more efficiently with regard to <strong>nutrient</strong><br />
accumulation.<br />
References<br />
Briggs, M. R. P., and Funge-Smith, S. J. 1994. A <strong>nutrient</strong> budget of some<br />
<strong>in</strong>tensive mar<strong>in</strong>e shrimp ponds <strong>in</strong> Thailand. Aquacult. Fisheries Manage.<br />
25:789-811.<br />
Chiang, Y. M. 1993. Seaweed cultivation <strong>in</strong> Taiwan. In Liao, I. C., Cheng, J. H.,<br />
Wu, M. C., Guo, J. J. (Eds.) Proc. Symp. On Aquaculture held <strong>in</strong> Beij<strong>in</strong>g,<br />
21-23 December 1992. Taiwan Fisheries Research <strong>Institut</strong>e, Keelung, pp.<br />
143-51<br />
Edward, P. 1992. Reuse of human wastes <strong>in</strong> <strong>aquaculture</strong>, a technical review.<br />
Water and sanitation report no 2. UNDP-World Bank Sanitation Program.<br />
World Bank. Wash<strong>in</strong>gton, DC. Pp, 33-50.<br />
Funge-Smith, S. J. and M. R. P. Briggs. 1998. Nutrient budgets <strong>in</strong> <strong>in</strong>tensive<br />
shrimp ponds: implications for susta<strong>in</strong>ability. Aquaculture. 164. 117-133.<br />
Harrison, P. J., and Hurd, C. L. 2001. Nutrient physiology of seaweeds:<br />
application of concepts to <strong>aquaculture</strong>. Cah. Biol. Mar. 42:71-82<br />
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Ihsan, Y. N, K. J. Hesse, N Holmgren, C Schulz. Submitted. A Comparison of<br />
Nutrients Fluxes <strong>in</strong> Monoculture and Polyculture Systems for Shrimp<br />
(Penaeus vannamei) and Seaweed (Gracillaria verrucosa) Production.<br />
Submitted to the journal of World Aquaculture Society.<br />
Lombardi, J. V., de Almeida-Marques, H. L., Pereira, R. T. L., Barreto, O. J. S.,<br />
de Paula, E. J. 2006. Cage polyculture of the Pacific white shrimp<br />
Litopenaeus vannamei and the Philipp<strong>in</strong>es seaweed Kappaphycus<br />
alvarezii. J. Aquacult. 258:412-415.<br />
Neori, A., Ragg, N. L.C., Shpigel, M. 1998. The <strong>in</strong>tegrated culture of seaweed,<br />
abalone, fish and clams <strong>in</strong> modular <strong>in</strong>tensive land-based <strong>systems</strong>: II.<br />
Performance and nitrogen partition<strong>in</strong>g with<strong>in</strong> an abalone (Haliotis<br />
tuberculata) and macroalgae culture system. Aquacult. Eng. 17:215-239.<br />
Neori, A., T. Chop<strong>in</strong> T, M. Troell, A. H. Buschmann, G.P. Kraemer, C. Hall<strong>in</strong>g,<br />
M. Shpigel, C Yarish. 2004. Integrated <strong>aquaculture</strong>: rationale, evolution<br />
and state of the art emphasiz<strong>in</strong>g seaweed biofiltration <strong>in</strong> modern<br />
mariculture. Aquaculture 231:361–391.<br />
Qian, P. Y., C. Y. Wu, M. Wu, Y. K. Xie. 1996. Integrated cultivation of red alga<br />
Kappaphycus alvarezii and the pearl oyster P<strong>in</strong>ctada martensi.<br />
Aquaculture 147: 21-35<br />
Schuenhoff, A., Shpigel, M., Lupatsch, I., Ashkenazi, A., Msuya, F. E., Neori, A.<br />
2003. A semi-recirculat<strong>in</strong>g, <strong>in</strong>tegrated system for the culture of fish and<br />
seaweed. Aquaculture 221:167–181.<br />
Soriano, E. M., C Morales, W. S. C Moreira. 2002. Cultivation of Gracillaria<br />
(Rhodophyta) <strong>in</strong> shrimp pond effluents <strong>in</strong> Brazil. Aquaculture Research<br />
33: 1081-1086.<br />
Tacon, A. G. J. 2002. Thematic review of feed and feed management practices <strong>in</strong><br />
shrimp <strong>aquaculture</strong>. Report prepared under the World Bank, NACA,<br />
WWF and FAO consortium program on shrimp farm<strong>in</strong>g and the<br />
environment, published by consortium. 69.<br />
Troell, M., C Hall<strong>in</strong>g, A Nilsson, A. H Buschmann., N Kautsky, L Kautsky. 1997.<br />
Integrated mar<strong>in</strong>e cultivation of Gracilaria chilensis (Gracilariales,<br />
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Bangiophyceae) and salmon cages for reduced environmental impact and<br />
<strong>in</strong>creased economic output. Aquaculture 156:45–61.<br />
Xu, Y. J., N. Z. Jiao, L. M. Qian. 2004. Nitrogen nutritional identities of<br />
Gracillaria as bio<strong>in</strong>dicators and restoral plants (<strong>in</strong> Ch<strong>in</strong>ese with English<br />
abstract). Journal of Fishery Sciences of Ch<strong>in</strong>a. 11. 276-281.<br />
Xu, Y. J., J. Fang, Q. Tang, J. L<strong>in</strong>, G. Le. 2008. Improvement of water quality by<br />
the macroalga, Gracillaria lemaneiformis (Rhodophyta), near <strong>aquaculture</strong><br />
effluent outlets. World <strong>aquaculture</strong> society. 39. 549-555.<br />
101
General Summary<br />
Feed based shrimp and fish <strong>aquaculture</strong> produces a large amount of waste,<br />
<strong>in</strong>clud<strong>in</strong>g nitrogen and phosphorus that is released to the aquatic environment<br />
without treatment. The present thesis is focussed on various polyculture <strong>systems</strong><br />
us<strong>in</strong>g shrimp Penaeus vannamei, fish Oreochromis sp. and seaweed Gracillaria<br />
verrucosa. Seaweed cultivation <strong>in</strong> <strong>in</strong>tegrated polyculture system appears to be a<br />
viable approach to reduce <strong>nutrient</strong>s discharge to the environment. Seaweed can be<br />
efficient <strong>in</strong> remov<strong>in</strong>g <strong>nutrient</strong>s from effluents of <strong>in</strong>tensive fish and shrimp farm.<br />
By <strong>in</strong>tegrat<strong>in</strong>g fed with extractive forms of <strong>aquaculture</strong>, the wastes of one<br />
resource user become a source for the others.<br />
Chapter one presents an <strong>in</strong>troduction of <strong>nutrient</strong> <strong>fluxes</strong> <strong>in</strong> various polyculture<br />
<strong>systems</strong> and implication for its susta<strong>in</strong>ability. A review of scientific literature<br />
illustrates important aspects to implement polyculture system us<strong>in</strong>g seaweed as<br />
biofilter. The production of seaweed <strong>in</strong> cage culture can be successfully <strong>in</strong>tegrated<br />
<strong>in</strong> the production of fish and shrimp. Regard<strong>in</strong>g the environmental benefits of<br />
<strong>in</strong>tegrated seaweed and fish or shrimp production, seaweed culture can also<br />
benefit by <strong>in</strong>creas<strong>in</strong>g their economic viability. Integrated seaweed <strong>aquaculture</strong><br />
<strong>systems</strong> have been suggested as a possible solution for secur<strong>in</strong>g an <strong>in</strong>creas<strong>in</strong>g and<br />
environmentally sounded production of future supply of fish and seafood.<br />
Chapter two compares performance and <strong>nutrient</strong> <strong>fluxes</strong> of monoculture and<br />
polyculture system. Therefore triplicate ponds of 1200 m² were stocked with<br />
seaweed (0.04 kg/m²) and 20 <strong>in</strong>dividuals of shrimp (0.22 ± 0.016 g/<strong>in</strong>d)/m 2 . The<br />
culture period lasted 100 days and water samples to describe <strong>nutrient</strong> <strong>fluxes</strong> were<br />
taken every 10 days. Results <strong>in</strong>dicate that polyculture <strong>systems</strong> us<strong>in</strong>g seaweed<br />
seem to act more efficiently with regard to <strong>nutrient</strong> accumulation. The average<br />
ammonium-nitrogen concentration over the whole period was 0.24 mg/l <strong>in</strong><br />
polyculture while <strong>in</strong> monoculture 0.37 mg/l of ammonium-nitrogen were<br />
analyzed. From the total nitrogen and total phosphorus <strong>in</strong>put, 24.2% and 5.3%<br />
were <strong>in</strong>corporated <strong>in</strong> 335.7 kg/1200 m 2 shrimp weight ga<strong>in</strong> <strong>in</strong> monoculture, while<br />
30.8% and 6.9% were <strong>in</strong>corporated <strong>in</strong> 501.5 kg/1200m 2 shrimp weight ga<strong>in</strong> and<br />
102
3.5% and 2.4% were <strong>in</strong>corporated <strong>in</strong> 325 kg/1200 m 2 seaweed <strong>in</strong> polyculture<br />
system.<br />
A comparative study on polyculture <strong>systems</strong> us<strong>in</strong>g various comb<strong>in</strong>ations of<br />
shrimp, seaweed and fish was conducted <strong>in</strong> chapter three <strong>in</strong> order to calculate<br />
<strong>nutrient</strong>s <strong>fluxes</strong> and mass balances. Therefore, triplicate ponds of 1000 m 2 size<br />
were stocked with 0.4 kg/m 2 seaweed and 15 shrimps/m 2 (polyculture I), and<br />
triplicate ponds of size 1000 m 2 were stocked with 0.4 kg/m 2 seaweed, 15<br />
shrimps/m 2 , and 0.25 fish/m 2 (polyculture II). A mass balance model was<br />
developed for total nitrogen and total phosphorus to estimate their <strong>fluxes</strong>. From<br />
total nitrogen and total phosphorus <strong>in</strong>put, 46.79% and 14.99% were <strong>in</strong>corporated<br />
<strong>in</strong> 313.08 kg/1000 m 2 shrimp weight ga<strong>in</strong> <strong>in</strong> polyculture system I, while 41.47%<br />
and 13.47% were <strong>in</strong>corporated <strong>in</strong> 291.25 kg/1000 m 2 shrimp weight ga<strong>in</strong> and<br />
13.64% and 5.09% were <strong>in</strong>corporated <strong>in</strong> 40.67 kg/1000 m 2 fish weight ga<strong>in</strong> <strong>in</strong><br />
polyculture system II. These results suggest that no significant differences <strong>in</strong><br />
shrimp performance between the two polyculture <strong>systems</strong> (P>0.05) could be<br />
observed.<br />
Chapter four evaluated the <strong>nutrient</strong> absorption efficiency of comb<strong>in</strong>ed shrimp and<br />
seaweed production. Therefore, triplicate concrete tanks, with a volume of 3 m 3 ,<br />
were stocked with shrimp (6–7 g, 5 <strong>in</strong>d/100 litres) and seaweed <strong>in</strong> densities of 0<br />
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<br />
<strong>in</strong> shrimp polyculture showed the highest ability for nitrogen assimilation<br />
orig<strong>in</strong>at<strong>in</strong>g from shrimp waste. This treatment <strong>in</strong>creased shrimp survival rate from<br />
63% (without seaweed) to 83% and the growth performance of shrimp from<br />
247.78 g (without seaweed) to 350.20 g. Rema<strong>in</strong><strong>in</strong>g nitrogen excreted by shrimp<br />
amounted to 15.36 g, which was ma<strong>in</strong>ly (14.62 g) utilized by seaweed to form a<br />
biomass of 16.90 kg. Therefore, polyculture <strong>systems</strong> us<strong>in</strong>g seaweed seem to act<br />
more efficiently with regard to <strong>nutrient</strong> accumulation and beneficial effects on cocultured<br />
organisms.<br />
103
Zusammenfassung<br />
Die futtermittelbasierte Aquakultur kann zu e<strong>in</strong>er Anreicherung von<br />
Stoffwechselendprodukten führen, die die Qualität des genutzten Gewässers<br />
erheblich bee<strong>in</strong>trächtigen können. In der vorliegenden Arbeit wurde deshalb die<br />
Reduzierung von Nährstoffemissionen der Aquakultur durch multitrophe<br />
Haltungssysteme untersucht. Hierzu wurden verschiedene Kulturverfahren von<br />
Tilapia, Shrimp und Makroalgen unter praxisgleichen Bed<strong>in</strong>gungen <strong>in</strong> Indonesien<br />
untersucht.<br />
Kapitel e<strong>in</strong>s der vorliegenden Arbeit führt thematisch e<strong>in</strong> und beschreibt die<br />
grundlegenden Prozesse im Nährstoffkreislauf von Gewässer- und<br />
Aquakultursystemen. Aufgrund der vielfältigen gelösten und partikulären<br />
Nährstofffraktionen <strong>in</strong> Aquakultursystemen kann nur auf Basis von multitrophen<br />
Systemen e<strong>in</strong>e relevante Nährstoffausnutzung realisiert werden. Anhand vieler<br />
Untersuchungen aus der Literatur kann dabei auf die besondere Bedeutung von<br />
Algen als Biofilter <strong>in</strong> e<strong>in</strong>em Polykultur-System h<strong>in</strong>gewiesen werden, da deren<br />
hohe Wachstumspotentiale die anfallenden gelösten Stickstoff- und<br />
Phosphorverb<strong>in</strong>dungen der tierischen Aquakulturproduktion effektiv verwerten,<br />
die Haltungsumwelt <strong>für</strong> weitere Organismen optimieren und der zusätzlichen<br />
ökonomischen Wertschöpfung dienen. Weiterh<strong>in</strong> bietet sich die komb<strong>in</strong>ierte<br />
Aufzucht von carnivoren mit omni- oder herbivioren Species an, da somit die<br />
Stoffwechselendprodukte <strong>in</strong> der niedrigeren Trophieebene effektiv <strong>in</strong> Biomasse<br />
überführt werden können.<br />
In Kapitel zwei werden die Potentiale von Monokultur- und Polykultursysteme<br />
experimentell mite<strong>in</strong>ander verglichen. Da<strong>für</strong> wurden drei Teiche mit identischer<br />
Fläche von 1200 m 2 <strong>in</strong> Polykultur mit Gracillaria verrucosa (50 kg) und 20<br />
Shrimps/m² (Penaeus vannamei, Anfangsgewicht 0.22 ± 0.016 g) besetzt.<br />
Weiterh<strong>in</strong> dienten 3 Teiche mit Shrimpmonokultur bei Besatzdichten von 20<br />
Shrimps/m² als Vergleich. Der Versuch wurde über 100 Tage durchgeführt und im<br />
Abstand von 10 Tagen wurden die Wasser<strong>in</strong>haltsstoffe erfasst. Die Werte<br />
<strong>in</strong>dizieren, dass das Polykultur-System mit Algen Gracillaria effizienter die<br />
zugeführten Nährstoffe <strong>in</strong> Biomasse überführen. Die Durchschnittskonzentration<br />
104
von Ammonium-Stickstoff über die gesamte Versuchsperiode betrug<br />
beispielsweise 0.24 mg/l im Polykultur- und 0.37 mg/l im Monokultursystem. In<br />
der Nährstoffbilanzierung zeigt sich, dass aus dem gesamten Stickstoff (TN)- und<br />
Phospore<strong>in</strong>trag (TP) 24.2% bzw. 5.3% <strong>in</strong> 335.7 kg Shrimpsbiomasse <strong>in</strong> der<br />
Monokultur überführt wurde, während <strong>in</strong> der Polykultur 30.8% bzw. 6.9% des<br />
e<strong>in</strong>getragenen TN und TP <strong>in</strong> 501.5 kg Shrimps und 3.5 % bzw. 2.4% des TN und<br />
TP <strong>in</strong> 325 kg Makroalgen Gracillaria verrucosa e<strong>in</strong>gebaut wurden.<br />
Im dritten Kapitel wurden das Polykulturverfahren mit Gracillaria-Algen und<br />
Shrimp (Peneaus vannamei, Polykultur I) mit e<strong>in</strong>em dreigliedrigen Verfahren aus<br />
Shrimp (Peneaus vannamei), Fisch (Oreochromis niloticus) und Makroalgen<br />
(Gracillaria verrucosa, Polykultur II) verglichen. Hier<strong>für</strong> wurde wiederum e<strong>in</strong><br />
triplikater Versuchsansatz mit jeweils drei Teichen mit e<strong>in</strong>er Fläche von 1000 m 2<br />
e<strong>in</strong>gesetzt und mit 0.4 kg/m 2 Makroalgen und 15 Shrimps/m 2 besetzt. In die<br />
dreigliedrigen Polykultursystemteiche wurden zusätzlich 0.25 Fische/m² gesetzt.<br />
Das Fütterungsmanagement berücksichtigte lediglich die Shrimps, die <strong>in</strong> beiden<br />
Versuchsansätzen mit vergleichbarer Intensität gefüttert wurden. In der<br />
Nährstoffbilanz zeigte sich, dass <strong>in</strong> Polykultur I aus dem TN- und TP-E<strong>in</strong>trag<br />
46.70% und 14.99% <strong>in</strong> 313.08 kg Shrimpbiomasse umgesetzt wurde, während <strong>in</strong><br />
Polykultur II 41.7% und 13.47% <strong>in</strong> 291.25 kg Shrimps und 13.62% und 5.09% <strong>in</strong><br />
40.67 kg m 2 Fisch e<strong>in</strong>gebaut wurden. Die Makroalgen <strong>in</strong>korporierten <strong>in</strong><br />
Polykultur I 10.56 % und 9.75 % TN und TP, und <strong>in</strong> Polykultur II vergleichbare<br />
10.94% und 8.83%. Dieses Ergebnis zeigt, dass das Shrimpsaufkommen durch die<br />
Polykultur mit Fischen nicht signifikant bee<strong>in</strong>trächtigt wird, durch die zusätzliche<br />
Nährstoffb<strong>in</strong>dung jedoch signifikant weniger Nährstoffe aus dem System geführt<br />
werden.<br />
Im abschließenden vierten Kapitel wurde das Nährstoffaufnahmepotential von<br />
variierendem Makroalgenbesatz <strong>in</strong> Polykultur mit Shrimps untersucht. Da<strong>für</strong><br />
wurden <strong>in</strong> kle<strong>in</strong>skaligen Betonsystemen mit e<strong>in</strong>em Volumen von 3 m 3 Garnelen,<br />
Penaeus vannamei, (6-7 g, 5 Ind/100 Liter) und Makroalgen Gracillaria<br />
verrucosa bei verschiedenen Kulturdichten von 0 g/l, 3.125 g/l, 6.250 g/l und<br />
9.375 g/l aufgezogen und die Wachstumsleistungen und Nährstoffbilanzen<br />
105
ermittelt. Dabei zeigte sich, dass die Stickstoffaufnahme der Makroalgen bei e<strong>in</strong>er<br />
Besatzdichte von 3.<br />
125 g/l am höchsten ist. Zudem kann e<strong>in</strong>e positive Wirkung auf die Shrimps<br />
festgestellt werden, da sich höhere Wachstumsleistungen (Gesamtendgewicht:<br />
243.78 g ohne Algen; 350.20 g bei Algendichte: 3.125 g/l) und<br />
Überlebensleistungen der Shrimps (63% ohne Algen, 83% bei Algendichte von<br />
3.125 g/l) e<strong>in</strong>stellen. Der aus der Shrimpfütterung stammende Stickstoff (15.36 g)<br />
wurde dabei überwiegend (14.62 g) von den Algen zur Biomassebildung genutzt.<br />
Schlussfolgend kann gesagt werden, dass die gezielte Polykultur von Shrimps-,<br />
Fisch und Makroalgenaufzucht zu e<strong>in</strong>er deutlich verbesserten<br />
Nährstoffausnutzung und damit zu ger<strong>in</strong>geren Nährstoffausträgen aus<br />
Aquakulturen führen können. Die Zusammenhänge zwischen den<br />
unterschiedlichen trophischen Produktionsebenen s<strong>in</strong>d jedoch nur <strong>in</strong> Teilen<br />
verstanden, so dass weiterh<strong>in</strong> e<strong>in</strong> sehr großes Optimierungspotential besteht.<br />
106
Danksagung<br />
An dieser Stelle möchte ich den Menschen Dank entgegenbr<strong>in</strong>gen, die zum<br />
Gel<strong>in</strong>gen der vorliegenden Arbeit beigetragen haben.<br />
Ich bedanke mich bei me<strong>in</strong>em Betreuer Herrn Prof. Dr. Carsten Schulz <strong>für</strong> die<br />
Überlassung des <strong>in</strong>teressanten Themas und das mir geschenkte Vertrauen bei der<br />
Projektbearbeitung.<br />
Herrn Dr. Karl J. Hesse vom FTZ-Buesum und Prof. Dr. Nöel Holmgren der<br />
Universität zu Skövde-Sweden danke ich <strong>für</strong> die Diskussion.<br />
Dank gilt me<strong>in</strong>en lieben Kolleg<strong>in</strong>nen und Kollegen vom FTZ/Corelab <strong>für</strong> die<br />
Unterstützung bei der Versuchsdurchführung und die überaus schöne Zeit <strong>in</strong> Kiel<br />
und Büsum. Besonders bei Herrn Prof. Dr. Roberto Mayerle, Dr. Peter Weppen,<br />
Britta Egge und Daniela Koch bedanke ich mich, dass ich als Gast <strong>in</strong> FTZ/Corelab<br />
arbeiten durfte.<br />
Den Kollegen aus Indonesien danke ich <strong>für</strong> die gute Zusammenarbeit.<br />
Ich bedanke mich bei Herrn Dede Suhendar <strong>für</strong> die Hilfsbereitschaft bei der<br />
Versuchsdurchführung und die angenehme Büronachbarschaft.<br />
Me<strong>in</strong>en Eltern danke ich <strong>für</strong> die wie immer selbstlose Unterstützung jeglicher Art.<br />
Und ganz besonders danke ich euch, Am<strong>in</strong>udd<strong>in</strong> Shaleh und Mulyati Am<strong>in</strong>udd<strong>in</strong>,<br />
weil ihr mir allzeit Kraft gebt<br />
Me<strong>in</strong> größter Dank an me<strong>in</strong>e Frau Tri Dewi K P und me<strong>in</strong>e K<strong>in</strong>der, Azka Auliya<br />
Yudanegara, Gilang Auliya Fauz<strong>in</strong> und Fadhlan Auliya Danurdoro <strong>für</strong> ihre<br />
Unterstützung.<br />
107
Name: Yudi Nurul Ihsan<br />
Geburstag: 1.12.1975<br />
Lebenslauf<br />
Gebursort: Bandung – Indonesien<br />
Eltern: Am<strong>in</strong>udd<strong>in</strong> Shaleh<br />
Schulausbildung:<br />
Mulyati Am<strong>in</strong>udd<strong>in</strong><br />
1982-1988 SD Melong Asih II Bandung - Indonesien<br />
1988-1994<br />
Studium:<br />
SMAM Garut - Indonesien<br />
1994-1999 Bachelor-Studium “Aquaculture“ an der Bogor Agricultural<br />
University zu Bogor (IPB-Bogor) Indonesien<br />
1999-2002 Master-Studium “Coastal and Mar<strong>in</strong>e Resource<br />
Management“ an der Bogor Agricultural University zu<br />
Bogor (IPB-Bogor) Indonesien<br />
Berufliche Tätigkeit:<br />
2002-2005 Wissenschaftliche Mitarbeiter am Center for Coastal and<br />
Mar<strong>in</strong>e Resources Study (CCMRS-IPB) Bogor, Indonesien<br />
2005-2008 Wissenschaftliche Mitarbeiter an der Fisheries and Mar<strong>in</strong>e<br />
Sciences Fakultät, Universitas Padjadjaran Bandung,<br />
Indonesien<br />
2008-2011 Wissenschaftliche Mitarbeiter bei der Gesellschaft <strong>für</strong><br />
Mar<strong>in</strong>e Aquakultur (GMA) mbH <strong>in</strong> Büsum bei Herrn Prof.<br />
Dr. C. Schulz<br />
108