Main Article Content
Abstract
Interest is increasing in Integrated Multi-Trophic Aquaculture Systems (IMTA) that encourage the development of environmentally friendly practices. By combining fed aquaculture with nearby extractive aquaculture, an IMTA can minimize the negative ecological impacts of conventional monoculture farms while expanding their economic base. To evaluate the efficiency of such a system, we applied dynamic STELLA modeling based on nitrogen content. The application of seaweed co-culturing reduced the level of dissolved inorganic nitrogen (DIN) by 20 to 35% over the short term whereas DIN values declined annually by 68 to 88%. When sea cucumber was incorporated into the scheme, the amount of particulate organic nitrogen was decreased by up to 50%. Ultimately, we plan to introduce potential strategic guidelines for IMTA implementation that might improve management and predictive capabilities while enhancing the social acceptability of such a system.
Keywords
Article Details
Copyright (c) 2015 Aquacultura Indonesiana

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
- Bouwman, L., A. Beusen, P.M. Glibert, C.Overbeek, M. Pawlowski, J. Herera, S.Muslow, R. Yu, and M. Zhou. 2013. Mariculture: significant and expanding cause of coastal nutrient enrichment. Environmental Research Letters, 8:1-5
- Bolliet, V., M. Azzaydi, and T. Boujard. 2001. Effect of feeding time on feed intake and growth. In D. Houlihan,T. Boujard and M. Jobling (Eds) Food Intake in Fish. Blackwell Publishing Company, Oxford UK. pp 233-249
- Broch, J.B. and D. Slagstad. 2012. Modelling seasonal growth and composition of the kelp Saccharina latisima. Journal of Applied Phycology, 24:759-776
- Buschmann, A.H., M. Troell, N. Kautsky, and L. Kautsky. 1996. Integrated tank cultivation of salmonids and Gracilaria chilensis (Gracilariales Rhodophyta). Hydrobiologia, 326/327:75-82
- Buschmann, A.H., F. Cabello, K. Young, J. Carvajal, D.A. Varela, and L. Henriquez. 2009. Salmon aquaculture and ecosystem health in Chile: analysis and regulation, environmental impact and bioremediation systems. Ocean and Coastal Management, 52:243-249
- Carmona, R., G.P. Kraemer, and C. Yarish. 2006.
- Exploring Northeast American and Asian species of Porphyra for use in an integrated finfish-algal aquaculture system. Aquaculture, 252:54-65
- Castine, S.A., A.D. McKinnon, N.A. Paul, L.A.
- Trott, and R. de Nys. 2013. Review. Waste
- water treatment for land-based aquaculture:
- improvement and value-adding alternatives in
- model system from Australia. Aquaculture
- Environment and Interaction, 4:285-300
- Chopin, T. 2011. Progression of the integrated multi
- trophic aquaculture (IMTA) concept and
- upscaling of IMTA system towards
- commercialization. Aquaculture Europe, 36 (4):5-12
- Chopin, T. 2013. Aquaculture, integrated multi
- trophic (IMTA). In R.A. Meyers (Ed) Encyclopedia of Science and Technology,12:542-564
- Chopin, T., A.H. Buschmann, C. Halling, M.
- Troell, N. Kautsky, A. Neori, G.P.
- Kraemer, J.A.Z. Gonzales, C. Yarish, and
- C. Neefus. 2001. Integrating seaweed into
- marine aquaculture system: a key toward
- sustainability. Journal of Phycology, 37:975-986
- Chopin, T., J. Cooper, G. Reid, S. Cross, and C.
- Moore. 2012. Open water integrated multi
- tropic aquaculture: environment
- biomitigation and economic diversification of
- fed aquaculture by extractive aquaculture.
- Review of Aquaculture, 4:209-220
- Chung, I.K., Y.H. Kang, C. Yarish, G.P. Kraemer,
- and J.A. Lee. 2002. Application of seaweed
- cultivation to the bioremediation of nutrient-
- rich effluent. Algae, 17(3):1-10
- Chung, I.K., J. Beardall, S. Mehta, D. Sahoo, and
- S. Stojkovic. 2011. Using marine macroalgae
- for carbon sequestration. A critical appraisal.
- Journal of Applied Phycology, 23:877-886
- Cohen, I. and A. Neori. 1991. Ulva lactuca biofilter
- for marine fish pond effluent I ammonium
- uptake kinetics and nitrogen content.
- Botanica Marina, 34:141-149
- Costanza, R. and A. Voinov. 2001. Modeling
- ecological and economic systems with
- STELLA: Part III. Ecological Modeling,
- :1-7
- Cotton, C.F., R.I. Walker, and T.C. Recicar. 2003.
- Effect of temperature & salinity on growth of
- juvenile black sea bass with implication for
- aquaculture. North American Journal of
- Aquaculture, 65:330-338
- De Silva, S.S. 2012. Aquaculture: a newly emergent
- food production sector- and perspectives of
- its impacts on biodiversity and conservation.
- Biodiversity Conservation, 21:3187-3220
- Everett, J.D., M.E. Baird, and I.M. Suthers. 2007.
- Nutrient and plankton dynamics in an
- intermittently closed/open lagoon, Smiths
- Lake, south-eastern Australia: an ecological
- model. Estuarine, Coastal and Shelf Science,
- :690-702
- Folke, C. and N. Kautsky. 1989. The role of
- ecosystems for a sustainable aquaculture.
- Ambio 18:234-243
- Gowen, R.J. and N.B. Bradbury.1987. The
- ecological impact of salmonid farming in the
- coastal waters; a review. Oceanography and
- Marine Biology, 25:563-575
- Harrison, P.J. and C.I. Hurd. 2001. Nutrient
- physiology of seaweed: application of
- concept to aquaculture. Cahiers de Biologie
- Marine, 42:71-82
- Islam, M.S. 2005. Nitrogen and phosphorus budget in
- coastal and marine cage aquaculture and
- impact of nutrient loading on ecosystem:
- review and analysis towards model
- development. Marine Pollution Bulletin,
- :48-61.
- Lamprianidou, F., T. Telfer, and L.G. Ross. 2015.
- A model for optimization of the productivity
- and bioremediation efficiency of marine
- integrated multitrophic aquaculture.
- Estuarine, Coastal and Shelf Science,
- :253-264
- Le Ruyet, J.P., K. Mahe, N. Le Bayon, and H. Le
- Delliou. 2004. Effect of temperature on
- growth & metabolism in a Mediterranean
- population of European sea bass
- Dicantrarchus labrax. Aquaculture, 237:269-
- Macchiavello, J. and C. Bulboa. 2014. Nutrient
- uptake efficiency of Gracilaria chilensis and
- Ulva lactuca in an IMTA system with red
- abalone Haliostis rufescens. Latin American
- Journal of Aquatic Research, 42(3):523-533
- Navarrete-Mier, F., C. Sanz-Lazaro, and A.
- Martin. 2010. Does bivalve molusc
- polyculture reduce marine finfish farming
- environmental impact? Aquaculture,
- :101-107
- Nelson, E.J., B.A. Macdonald, and S.M.C.
- Robinson. 2012. The absorption efficiency of
- suspension feeding sea cucumber Cucumaria
- frondosa and its potential as an extractive
- integrated multi trophic aquaculture (IMTA)
- species. Aquaculture, 370-371:19-25
- Neori, A. and M.D. Krom. 1991. Nitrogen and
- phosphorus budget in an intensive marine
- fishpond; the importance of microplankton.
- In C.B. Cowey and C.Y. Cho. (Eds).
- Proceedings of First International
- Symposium on Nutritional Strategy in
- Management of Aquaculture Waste.
- University of Guelph, Ontario. pp 187-205
- Neori, A., M. Shpigel, and D. Ben-Ezra. 2000. A
- sustainable integrated system for culture fish,
- seaweed and abalone. Aquaculture, 186:279-
- Neori, A., M. Troell, T. Chopin, C. Yarish, A.
- Critchley, and A.H. Buschmann. 2007. The
- need for a balanced ecosystem approach to
- blue revolution aquaculture. Environment;
- Science & Policy for Sustainable
- Development, 49:36-43
- Nikolaisen, L., P.D. Jensen, K.S. Bech, J. Dahl, J.
- Busk, T. Brodsgaard, M.B. Rasmussen, A.
- Bruhn, A.B. Bjerre, H.B. Nielsen, K.R.
- Albert, P. Ambus, Z. Kader, S. Heiske, B.
- Sander, and E.R. Schmidt. 2011. Energy
- production for marine Biomass (Ulva Lactuca).
- PSO Project No. 2008-1-0050. pp 1-72
- Nizzoli, D., D.T. Welsh, M. Bartoli, and P. Viaroli.
- Impact of mussel (Mytilus
- galloprovincialis) farming on oxygen
- consumption and nutrient recycling in a
- eutrophic coastal lagoon. Hydrobiologia,
- :183-198
- Ren, J.S., J.S. Dozey, D.R. Plew, J. Fang, and M.
- Gall. 2012. An ecosystem model for
- optimizing production in integrated multi
- trophic aquaculture systems. Ecological
- Modeling, 246:34-46
- Ridler, N., M. Wowchuk, B. Robinson, K.
- Barrington, T. Chopin, S. Robinson, F.
- Page, G. Reid, M. Szemerda, J. Sewuster,
- and S.B. Travis. 2007. Integrated multi
- trophic aquaculture (IMTA) a potential
- strategic choice for farmers. Aquaculture
- Economics and Management, 11:99-110
- Rose, J. M., S.B. Bricker, M.A. Tedesco, and G.F.
- Wikfors. 2014. A role for shellfish
- aquaculture in coastal nitrogen management.
- Environment Science and Technology,
- :2519-2525
- Sara, G., G.K. Reid, A. Rinaldi, V. Palmer, M.
- Troell, and S.A.L.M. Kooijman. 2012.
- Growth and reproduction simulation of
- candidate shellfish species at fish cage in
- southern mediterranean; dynamic energy budget
- (DEB) modeling for integrated multi trophic
- aquaculture. Aquaculture, 324-325:259-266
- Schuenhoff, A., M. Shpigel, I. Lupatasch, A.
- Ashkenazi, F.E. Msuya, and A. Neori.
- A semi recirculating, integrated system
- for culture of fish and seaweed. Aquaculture,
- :167-181
- Shpigel, M., A. Neori, M.D. Popper, and H.
- Gordin. 1993. A proposed model for
- “environmentally clean” land -based culture
- of fish, bivalve and seaweed. Aquaculture,
- :115-128
- Slater, M.J. and A.G. Carton. 2007. Survivorship
- and growth of the sea cucumber
- Australostichopus (Stichopus) mollis (Hutton
- in polyculture trials with green lipped
- mussel farm. Aquaculture, 272:389-398
- Troell, M., N. Kautsky, and C. Folke. 1999.
- Applicability of integrated coastal
- aquaculture system. Ocean and Coastal
- Management, 42:63-69
- Troell, M., A. Joyce, T. Chopin, A. Neori, A.H.
- Buschmann, and J.G. Fang. 2009.
- Ecological engineering in aquaculture
- potential for integrated multi trophic
- aquaculture (IMTA) in marine offshore
- system. Aquaculture, 297(1-4):1-9
- Wang, X., L.M. Olsen, K.I. Reitan, and Y. Olsen.
- Discharge of nutrient waste from
- salmon farms: environmental effect and
- potential for integrating multi trophic
- aquaculture. Aquaculture Environment and
- Interaction, 2:267-283
- Wu, H., Y. Huo, F. Han, Y. Liu, and P. He. 2015.
- Bioremediation using Gracilaria chouae co-
- culture with Sparus macrochephalus to
- manage the nitrogen and phosphorus balance
- in an IMTA system in Xiangshan Bay, China.
- Marine Pollution Bulletin, 91:272-279
- Wu, R.S.S. 1995. The environmental impact of
- marine fish culture: towards a sustainable
- future. Marine Pollution Bulletin, 31:159-166
- WWF Indonesia. 2014. Better management practice:
- budidaya rumput laut Gracilaria sp. di
- tambak. Panduan Perikanan Skala Kecil,
- hlm.1-32
- Xu, Z., X. Lin, Q. Lin, Y. Yang, and Y. Wang.
- Nitrogen, phosphorus and energy waste
- output of four marine cage culture fish fed
- with trash fish. Aquaculture, 263:130-141
- Yang, Y., Z. Chai, Q. Wang, W. Chen, Z. He, and S.
- Jiang. 2015. Cultivation of seaweed gracilaria
- in Chinese coastal waters and its contribution to
- environmental improvements. Algal Research,
- :236-244
References
Bouwman, L., A. Beusen, P.M. Glibert, C.Overbeek, M. Pawlowski, J. Herera, S.Muslow, R. Yu, and M. Zhou. 2013. Mariculture: significant and expanding cause of coastal nutrient enrichment. Environmental Research Letters, 8:1-5
Bolliet, V., M. Azzaydi, and T. Boujard. 2001. Effect of feeding time on feed intake and growth. In D. Houlihan,T. Boujard and M. Jobling (Eds) Food Intake in Fish. Blackwell Publishing Company, Oxford UK. pp 233-249
Broch, J.B. and D. Slagstad. 2012. Modelling seasonal growth and composition of the kelp Saccharina latisima. Journal of Applied Phycology, 24:759-776
Buschmann, A.H., M. Troell, N. Kautsky, and L. Kautsky. 1996. Integrated tank cultivation of salmonids and Gracilaria chilensis (Gracilariales Rhodophyta). Hydrobiologia, 326/327:75-82
Buschmann, A.H., F. Cabello, K. Young, J. Carvajal, D.A. Varela, and L. Henriquez. 2009. Salmon aquaculture and ecosystem health in Chile: analysis and regulation, environmental impact and bioremediation systems. Ocean and Coastal Management, 52:243-249
Carmona, R., G.P. Kraemer, and C. Yarish. 2006.
Exploring Northeast American and Asian species of Porphyra for use in an integrated finfish-algal aquaculture system. Aquaculture, 252:54-65
Castine, S.A., A.D. McKinnon, N.A. Paul, L.A.
Trott, and R. de Nys. 2013. Review. Waste
water treatment for land-based aquaculture:
improvement and value-adding alternatives in
model system from Australia. Aquaculture
Environment and Interaction, 4:285-300
Chopin, T. 2011. Progression of the integrated multi
trophic aquaculture (IMTA) concept and
upscaling of IMTA system towards
commercialization. Aquaculture Europe, 36 (4):5-12
Chopin, T. 2013. Aquaculture, integrated multi
trophic (IMTA). In R.A. Meyers (Ed) Encyclopedia of Science and Technology,12:542-564
Chopin, T., A.H. Buschmann, C. Halling, M.
Troell, N. Kautsky, A. Neori, G.P.
Kraemer, J.A.Z. Gonzales, C. Yarish, and
C. Neefus. 2001. Integrating seaweed into
marine aquaculture system: a key toward
sustainability. Journal of Phycology, 37:975-986
Chopin, T., J. Cooper, G. Reid, S. Cross, and C.
Moore. 2012. Open water integrated multi
tropic aquaculture: environment
biomitigation and economic diversification of
fed aquaculture by extractive aquaculture.
Review of Aquaculture, 4:209-220
Chung, I.K., Y.H. Kang, C. Yarish, G.P. Kraemer,
and J.A. Lee. 2002. Application of seaweed
cultivation to the bioremediation of nutrient-
rich effluent. Algae, 17(3):1-10
Chung, I.K., J. Beardall, S. Mehta, D. Sahoo, and
S. Stojkovic. 2011. Using marine macroalgae
for carbon sequestration. A critical appraisal.
Journal of Applied Phycology, 23:877-886
Cohen, I. and A. Neori. 1991. Ulva lactuca biofilter
for marine fish pond effluent I ammonium
uptake kinetics and nitrogen content.
Botanica Marina, 34:141-149
Costanza, R. and A. Voinov. 2001. Modeling
ecological and economic systems with
STELLA: Part III. Ecological Modeling,
:1-7
Cotton, C.F., R.I. Walker, and T.C. Recicar. 2003.
Effect of temperature & salinity on growth of
juvenile black sea bass with implication for
aquaculture. North American Journal of
Aquaculture, 65:330-338
De Silva, S.S. 2012. Aquaculture: a newly emergent
food production sector- and perspectives of
its impacts on biodiversity and conservation.
Biodiversity Conservation, 21:3187-3220
Everett, J.D., M.E. Baird, and I.M. Suthers. 2007.
Nutrient and plankton dynamics in an
intermittently closed/open lagoon, Smiths
Lake, south-eastern Australia: an ecological
model. Estuarine, Coastal and Shelf Science,
:690-702
Folke, C. and N. Kautsky. 1989. The role of
ecosystems for a sustainable aquaculture.
Ambio 18:234-243
Gowen, R.J. and N.B. Bradbury.1987. The
ecological impact of salmonid farming in the
coastal waters; a review. Oceanography and
Marine Biology, 25:563-575
Harrison, P.J. and C.I. Hurd. 2001. Nutrient
physiology of seaweed: application of
concept to aquaculture. Cahiers de Biologie
Marine, 42:71-82
Islam, M.S. 2005. Nitrogen and phosphorus budget in
coastal and marine cage aquaculture and
impact of nutrient loading on ecosystem:
review and analysis towards model
development. Marine Pollution Bulletin,
:48-61.
Lamprianidou, F., T. Telfer, and L.G. Ross. 2015.
A model for optimization of the productivity
and bioremediation efficiency of marine
integrated multitrophic aquaculture.
Estuarine, Coastal and Shelf Science,
:253-264
Le Ruyet, J.P., K. Mahe, N. Le Bayon, and H. Le
Delliou. 2004. Effect of temperature on
growth & metabolism in a Mediterranean
population of European sea bass
Dicantrarchus labrax. Aquaculture, 237:269-
Macchiavello, J. and C. Bulboa. 2014. Nutrient
uptake efficiency of Gracilaria chilensis and
Ulva lactuca in an IMTA system with red
abalone Haliostis rufescens. Latin American
Journal of Aquatic Research, 42(3):523-533
Navarrete-Mier, F., C. Sanz-Lazaro, and A.
Martin. 2010. Does bivalve molusc
polyculture reduce marine finfish farming
environmental impact? Aquaculture,
:101-107
Nelson, E.J., B.A. Macdonald, and S.M.C.
Robinson. 2012. The absorption efficiency of
suspension feeding sea cucumber Cucumaria
frondosa and its potential as an extractive
integrated multi trophic aquaculture (IMTA)
species. Aquaculture, 370-371:19-25
Neori, A. and M.D. Krom. 1991. Nitrogen and
phosphorus budget in an intensive marine
fishpond; the importance of microplankton.
In C.B. Cowey and C.Y. Cho. (Eds).
Proceedings of First International
Symposium on Nutritional Strategy in
Management of Aquaculture Waste.
University of Guelph, Ontario. pp 187-205
Neori, A., M. Shpigel, and D. Ben-Ezra. 2000. A
sustainable integrated system for culture fish,
seaweed and abalone. Aquaculture, 186:279-
Neori, A., M. Troell, T. Chopin, C. Yarish, A.
Critchley, and A.H. Buschmann. 2007. The
need for a balanced ecosystem approach to
blue revolution aquaculture. Environment;
Science & Policy for Sustainable
Development, 49:36-43
Nikolaisen, L., P.D. Jensen, K.S. Bech, J. Dahl, J.
Busk, T. Brodsgaard, M.B. Rasmussen, A.
Bruhn, A.B. Bjerre, H.B. Nielsen, K.R.
Albert, P. Ambus, Z. Kader, S. Heiske, B.
Sander, and E.R. Schmidt. 2011. Energy
production for marine Biomass (Ulva Lactuca).
PSO Project No. 2008-1-0050. pp 1-72
Nizzoli, D., D.T. Welsh, M. Bartoli, and P. Viaroli.
Impact of mussel (Mytilus
galloprovincialis) farming on oxygen
consumption and nutrient recycling in a
eutrophic coastal lagoon. Hydrobiologia,
:183-198
Ren, J.S., J.S. Dozey, D.R. Plew, J. Fang, and M.
Gall. 2012. An ecosystem model for
optimizing production in integrated multi
trophic aquaculture systems. Ecological
Modeling, 246:34-46
Ridler, N., M. Wowchuk, B. Robinson, K.
Barrington, T. Chopin, S. Robinson, F.
Page, G. Reid, M. Szemerda, J. Sewuster,
and S.B. Travis. 2007. Integrated multi
trophic aquaculture (IMTA) a potential
strategic choice for farmers. Aquaculture
Economics and Management, 11:99-110
Rose, J. M., S.B. Bricker, M.A. Tedesco, and G.F.
Wikfors. 2014. A role for shellfish
aquaculture in coastal nitrogen management.
Environment Science and Technology,
:2519-2525
Sara, G., G.K. Reid, A. Rinaldi, V. Palmer, M.
Troell, and S.A.L.M. Kooijman. 2012.
Growth and reproduction simulation of
candidate shellfish species at fish cage in
southern mediterranean; dynamic energy budget
(DEB) modeling for integrated multi trophic
aquaculture. Aquaculture, 324-325:259-266
Schuenhoff, A., M. Shpigel, I. Lupatasch, A.
Ashkenazi, F.E. Msuya, and A. Neori.
A semi recirculating, integrated system
for culture of fish and seaweed. Aquaculture,
:167-181
Shpigel, M., A. Neori, M.D. Popper, and H.
Gordin. 1993. A proposed model for
“environmentally clean” land -based culture
of fish, bivalve and seaweed. Aquaculture,
:115-128
Slater, M.J. and A.G. Carton. 2007. Survivorship
and growth of the sea cucumber
Australostichopus (Stichopus) mollis (Hutton
in polyculture trials with green lipped
mussel farm. Aquaculture, 272:389-398
Troell, M., N. Kautsky, and C. Folke. 1999.
Applicability of integrated coastal
aquaculture system. Ocean and Coastal
Management, 42:63-69
Troell, M., A. Joyce, T. Chopin, A. Neori, A.H.
Buschmann, and J.G. Fang. 2009.
Ecological engineering in aquaculture
potential for integrated multi trophic
aquaculture (IMTA) in marine offshore
system. Aquaculture, 297(1-4):1-9
Wang, X., L.M. Olsen, K.I. Reitan, and Y. Olsen.
Discharge of nutrient waste from
salmon farms: environmental effect and
potential for integrating multi trophic
aquaculture. Aquaculture Environment and
Interaction, 2:267-283
Wu, H., Y. Huo, F. Han, Y. Liu, and P. He. 2015.
Bioremediation using Gracilaria chouae co-
culture with Sparus macrochephalus to
manage the nitrogen and phosphorus balance
in an IMTA system in Xiangshan Bay, China.
Marine Pollution Bulletin, 91:272-279
Wu, R.S.S. 1995. The environmental impact of
marine fish culture: towards a sustainable
future. Marine Pollution Bulletin, 31:159-166
WWF Indonesia. 2014. Better management practice:
budidaya rumput laut Gracilaria sp. di
tambak. Panduan Perikanan Skala Kecil,
hlm.1-32
Xu, Z., X. Lin, Q. Lin, Y. Yang, and Y. Wang.
Nitrogen, phosphorus and energy waste
output of four marine cage culture fish fed
with trash fish. Aquaculture, 263:130-141
Yang, Y., Z. Chai, Q. Wang, W. Chen, Z. He, and S.
Jiang. 2015. Cultivation of seaweed gracilaria
in Chinese coastal waters and its contribution to
environmental improvements. Algal Research,
:236-244
