Biofiltering efficiency and productive performance of macroalgae with potential for integrated multi-trophic Aquaculture (IMTA)
Keywords:
Gracilaria birdiae, productivity, daily growth rate, nutrient removal, Ulva fasciata, Ulva flexuosaAbstract
Seaweeds have many uses in industry and agriculture and many species have potential for integrated multi-trophic aquaculture (IMTA), since they are efficient in removing nutrients from water. The efficiency of Ulva flexuosa, U. fasciata and Gracilaria birdiae in removing nutrients from enriched water and their productive performance in outdoor tanks were quantified. These seaweeds (50 g; n = 5) were grown in tanks containing 50 L of eutrophic seawater, with salinity of 30, temperature of 28.5 ± 2.8°C, irradiance of 547 ± 458 μmol photons m-2 s-1 and aeration. The nutrients levels were recorded daily and, when total nitrogen removal was detected, the biomass was measured. After five days of cultivation, more than 98% of NH3 (H = 1.1; P = 0.56) and NO3- (H = 2.7; P = 0.25) and 62.1% of PO43- (H = 0.0; P = 0.90) had been removed from the tanks. However, the mean daily growth rate (4.5 ± 2.5% day-1) and productivity (3.5 ± 1.9 g m-2 day-1) of U. fasciata and G. birdiae were higher than U. flexuosa (-13.6 ± 7.7% day-1; -6.24 ± 2.8 g m-2 day-1; P<0.01), demonstrating that microalga contamination by this species promoted high removal efficiency in the tanks, but a low productive performance. Based on these results, U. fasciata and G. birdiae show a greater potential for use in IMTA to improve water quality and produce biomass.
References
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biomass yield of the green seaweed, Ulva lactuca in an integrated marine aquaculture system at
the Red Sea coast of Saudi Arabia at different stocking densities and effluent flow rates. Reviews in Aquaculture, 7(3): 161-171.
ALMEIDA, C.L.F. de; FALCÃO, H. de S.; LIMA, G.R. de M.; MONTENEGRO, C. de A.; LIRA, N.S.;
ATHAYDE-FILHO, P.F. de; RODRIGUES, L.C.; SOUZA, M. de F.V. de; BARBOSA-FILHO, J.M.; BATISTA, L.M. 2011 Bioactivities from Marine Algae of the Genus Gracilaria. International Journal of Molecular Sciences, 12(7): 4550-4573.
ANÍBAL, J.; MADEIRA, H.T.; CARVALHO, L.F.;ESTEVES, E.; VEIGA-PIRES, C.; ROCHA, C. 2014 Macroalgae mitigation potential for fish aquaculture effluents: an approach coupling
nitrogen uptake and metabolic pathways using Ulva rigida and Enteromorpha clathrata.
Environmental Science and Pollution Research,21(23): 13324-13334.
BALOO, L.; AZMAN, S.; SAID, M.I.M.; AHMAD, F.; MOHAMAD, M. 2014 Biofiltration potential of
macroalgae for ammonium removal in outdoor tank shrimp wastewater recirculation system.
Biomass and Bioenergy, 66(1): 103-109.
BEAMISH, F.W.H. 1981 Swimming performance and metabolic rate of three tropical fishes in relation to temperature. Hydrobiologia, 83(2): 245-254.
BIXLER, H.J. and PORSE, H. 2011 A decade of change in the seaweed hydrocolloids industry.
Journal of Applied Phycology, 23(3): 321-335.
CAHILL, P.L.; LOKMAN, M.; HURD, C.L. 2010 Keeping the water clean: seaweed biofiltration
outperforms traditional bacterial biofilms in recirculating aquaculture. Aquaculture, 306(1-4):
153-159.
CASTELAR, B.; REIS, R.P.; CALHEIROS, A.C. dos S. 2014 Ulva lactuca and U. flexuosa (Chlorophyta,
Ulvophyceae) cultivation in Brazilian tropical waters: recruitment, growth, and ulvan yield.
Journal of Applied Phycology, 26(5): 1989-1999.
COPERTINO, M.D.; TORMENA, T.; SEELIGER, U. 2009 Biofiltering efficiency, uptake and V
assimilation rates of Ulva clathrata (Roth) J. Agardh (Chlorophyceae) cultivated in shrimp
aquaculture waste water. Journal of Applied Phycology, 21(1): 31-45.
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DAVIDSON, J.; GOOD, C.; WELSH, C.; BRAZIL, B.; SUMMERFELT, S. 2009 Heavy metal and waste
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45(1): 1-13.
MACCHIAVELLO, J.; BULBOA, C. 2014 Nutrient uptake efficiency of Gracilaria chilensis and Ulva
lactuca in an IMTA system with the red abalone Haliotis rufescens. Latin American Journal of
Aquatic Research, 42(3): 523-533.
MARINHO-SORIANO, E.; NUNES, S.O.; CARNEIRO, M.A.A.; PEREIRA, D.C. 2009 Nutrients removal
from aquaculture wastewater using the macroalgae Gracilaria birdiae. Biomass and Bioenergy, 33(2): 327-331.
MARINHO-SORIANO, E.; AZEVEDO, C.A.A.; TRIGUEIRO, T.G.; PEREIRA, D.C.; CARNEIRO,
M.A.A.; CAMARA, M.R. 2011 Bioremediation of aquaculture wastewater using macroalgae
and Artemia. International Biodeterioration & Biodegradation, 65(1): 253-257.
MARINHO, G.; NUNES C.; SOUSA-PINTO, I.;PEREIRA, R.; REMA, P.; VALENTE, L.M.P. 2013 The IMTA-cultivated Chlorophyta Ulva spp. as a sustainable ingredient in Nile tilapia (Oreochromis
niloticus) diets. Journal of Applied Phycology, 25(5): 1359-1367.
MARTINS, C.I.M.; EDING, E.H.; VERRETH, J.A.J. 2011 Stressing fish in Recirculating Aquaculture
Systems (RAS): does stress induced in one group of fish affect the feeding motivation of other fish
sharing the same RAS? Aquaculture Research,42(9): 1378-1384.
MARTINS, C.I.M.; EDING, E.H.; VERDEGEM, M.C.J.; HEINSBROEK, L.T.N.; SCHNEIDER, O.;
BLANCHETON, J.P.; ROQUE D’ORBCASTEL, E.; VERRETH, J.A.J. 2010 New developments in
recirculating aquaculture systems in Europe: A perspective on environmental sustainability.
Aquacultural Engineering, 43(3): 83-93.
MOURA, C.W.N. 2010 Ulvophyceae. In: FORZZA, R.C. Catálogo de plantas e fungos do Brasil. Vol. 1.
Rio de Janeiro: Andrea Jakobsson Estúdio,Instituto de Pesquisas Jardim Botí¢nico do Rio de Janeiro. p.438-448.
NEORI, A. 2008 Essential role of seaweed cultivation in integrated multi-trophic aquaculture farms
for global expansion of mariculture: an analysis.Journal of Applied Phycology, 20(5): 567í 570.
NEORI, A.; MSUYA, F.E.; SHAULI, L.;SCHUENHOFF, A.; KOPEL, F.; SHPIGEL, M.A. 2003 A novel three stage seaweed (Ulva lactuca) biofilter design for integrated mariculture. Journal of Applied Phycology, 15(6): 543í 553.
NIELSEN, M.M.; BRUHN, A.; RASMUSSEN, M.B.; OLESEN, B.; LARSEN, M.M.; MOLLER, H.B.
2012 Cultivation of Ulva lactuca with manure for simultaneous bioremediation and biomass
production. Journal of Applied Phycology, 24(3):449-458.
OLIVEIRA, V.P.; FREIRE, F.A.M.; MARINHOSORIANO, E. 2012 Influence of depth on the growth of the seaweed Gracilaria birdiae (Rhodophyta) in a shrimp pond. Brazilian Journal of Aquatic Science and Technology, 16(1): 33-39.
PEREIRA, R.; VALENTE, L.M.P.; SOUSA-PINTO, I.; REMA, P. 2012 Apparent nutrient digestibility of
seaweeds by rainbow trout (Oncorhynchus mykiss) and Nile tilapia (Oreochromis niloticus).
Algal Research, 1(1): 77-82.
PLASTINO, E.M. and OLIVEIRA, E.C. 2002 Gracilaria birdiae (Gracilariales, Rhodophyta), a new species from the tropical South American Atlantic with terete frond and deep spermatangial
conceptacles. Phycologia, 41(4): 389-396.
RAPOSO, D.; OLIVEIRA, S.R.; AFONSO, F.; FERNANDES, F.O.; MARINHO-SORIANO, E. 2014 Performance of shrimp Litopenaeus vannamei and seaweeds Gracilaria birdiae and Ulva fasciata
in an integrated multi-trophic aquaculture system. In: AQUACULTURE EUROPE, Trondheim, 2014. Anais... Trondheim: European Aquaculture Society.
ROSENTHAL, H.; CASTELL, J.D.; CHIBA, K.; FORSTER, J.R.M.; HILGE, V.; HOGENDOORN,H.; MAYO, R.D.; MUIR, J.F.; MURRAY, K.R.; PETIT, J.; WEDEMEYER, G.A.; WHEATON, F.;WICKINS, J. 1986 Flow-through and recirculation systems. EIFAC. 100p.
SODE, S.; BRUHN, A.; BALSBY, T.J.; LARSEN, M.M.; GOTFREDSEN,A.; RASMUSSEN, M.B.2013 Bioremediation of reject water anaerobically digested waste water sludge with macroalgae (Ulva lactuca, Chlorophyta).Bioresource Technology 146: 426-435.
VANDERMEULEN, H. and GORDIM, H. 1990 Ammonium uptake using Ulva (Chlorophyta) in
intensive fishpond systems: mass culture and treatment of effluent. Journal of Applied Phycology
2(4): 363-374.
VERDEGEM, M.C.J.; BOSMA, R.H.; VERRETH, J.A.J. 2005 Reducing water use for animal production
through aquaculture. International Journal of Water Resources Development, 22(1): 101-113.
YOKOYAMA, H. and ISHIHI, Y. 2010 Bioindicator and biofilter function of Ulva spp. (Chlorophyta)
for dissolved inorganic nitrogen discharged from a coastal fish farm - potential role in integrated
multi-trophic aquaculture. Aquaculture, 310(1-2): 74-83.
ZAR, J.H. 1996 Biostatistical analysis. New York:Prentice Hall, Upper Saddle River. 662p.
ZOHAR, Y.; TAL, Y.; SCHREIER, H.J.; STEVEN, C.;STUBBLEFIELD, J.; PLACE, A. 2005 Commercially
feasible urban recirculated aquaculture: addressing the marine sector. In: COSTA-PIERCE, B. Urban Aquaculture. Cambridge: CABI Publishing.p.159í 171.
biomass yield of the green seaweed, Ulva lactuca in an integrated marine aquaculture system at
the Red Sea coast of Saudi Arabia at different stocking densities and effluent flow rates. Reviews in Aquaculture, 7(3): 161-171.
ALMEIDA, C.L.F. de; FALCÃO, H. de S.; LIMA, G.R. de M.; MONTENEGRO, C. de A.; LIRA, N.S.;
ATHAYDE-FILHO, P.F. de; RODRIGUES, L.C.; SOUZA, M. de F.V. de; BARBOSA-FILHO, J.M.; BATISTA, L.M. 2011 Bioactivities from Marine Algae of the Genus Gracilaria. International Journal of Molecular Sciences, 12(7): 4550-4573.
ANÍBAL, J.; MADEIRA, H.T.; CARVALHO, L.F.;ESTEVES, E.; VEIGA-PIRES, C.; ROCHA, C. 2014 Macroalgae mitigation potential for fish aquaculture effluents: an approach coupling
nitrogen uptake and metabolic pathways using Ulva rigida and Enteromorpha clathrata.
Environmental Science and Pollution Research,21(23): 13324-13334.
BALOO, L.; AZMAN, S.; SAID, M.I.M.; AHMAD, F.; MOHAMAD, M. 2014 Biofiltration potential of
macroalgae for ammonium removal in outdoor tank shrimp wastewater recirculation system.
Biomass and Bioenergy, 66(1): 103-109.
BEAMISH, F.W.H. 1981 Swimming performance and metabolic rate of three tropical fishes in relation to temperature. Hydrobiologia, 83(2): 245-254.
BIXLER, H.J. and PORSE, H. 2011 A decade of change in the seaweed hydrocolloids industry.
Journal of Applied Phycology, 23(3): 321-335.
CAHILL, P.L.; LOKMAN, M.; HURD, C.L. 2010 Keeping the water clean: seaweed biofiltration
outperforms traditional bacterial biofilms in recirculating aquaculture. Aquaculture, 306(1-4):
153-159.
CASTELAR, B.; REIS, R.P.; CALHEIROS, A.C. dos S. 2014 Ulva lactuca and U. flexuosa (Chlorophyta,
Ulvophyceae) cultivation in Brazilian tropical waters: recruitment, growth, and ulvan yield.
Journal of Applied Phycology, 26(5): 1989-1999.
COPERTINO, M.D.; TORMENA, T.; SEELIGER, U. 2009 Biofiltering efficiency, uptake and V
assimilation rates of Ulva clathrata (Roth) J. Agardh (Chlorophyceae) cultivated in shrimp
aquaculture waste water. Journal of Applied Phycology, 21(1): 31-45.
CRUZ-SUÁREZ, E.L.; LEÓN, A.; PEí"˜A-RODRÍGUEZ, A.; RODRÍGUEZ-PEí"˜A, G.; MOLL, B.; RICQUEMARIE, D. 2010 Shrimp/Ulva co-culture: A sustainable alternative to diminish the need for
artificial feed and improve shrimp quality.Aquaculture, 301(1-4): 64í 68.
DAVIDSON, J.; GOOD, C.; WELSH, C.; BRAZIL, B.; SUMMERFELT, S. 2009 Heavy metal and waste
metabolite accumulation and their potential effect on rainbow trout performance in a replicated water reuse system operated at low or high system flushing rates. Aquacultural Engineering, 41(2): 136-145.
DAVIDSON, J.; GOOD, C.; WELSH, C.;SUMMERFELT, S.T. 2014 Comparing the effects of high vs. low nitrate on the health, performance, and welfare of juvenile rainbow trout Oncorhynchus mykiss within water recirculating aquaculture systems. Aquacultural Engineering, 59(1): 30í 40.
FAO. 2014 The State of World Fisheries and Aquaculture. 233 p. Available at: <http://www.fao.org/3/ai3720e.pdf> Access on: 30 Oct. 2014.
FLEURENCE, J. 1999 Seaweed proteins: biochemical,nutritional aspects and potential uses. Trends in Food Science & Technology, 10(1): 25-28.
GOOD, C.; DAVIDSON, J.; Welsh, C.; BRAZIL, B.;SNEKVIK, K.; SUMMERFELT, S. 2009 The impact of water exchange rate on the health and performance of rainbow trout Oncorhynchus mykiss in water recirculation aquaculture systems. Aquaculture, 294(1): 80-85.
GUIRY, M.D. and GUIRY, G.M. 2015 AlgaeBase. Available at: <http://www.algaebase.org>
Access on: 31 ago 2015.
HAYASHI, L.; YOKOYA, N. S.; OSTINI, S.; PEREIRA, R.T.L.; BRAGA, E.S.; Oliveira, E.C. 2008 Nutrients removed by Kappaphycus alvarezii (Rhodophyta, Solieriaceae) in integrated cultivation with fishes in recirculating water. Aquaculture, 277(3-4): 185-191.
KOEMAN, R.P.T. 1985 The taxonomy of Ulva Linnaeus, 1753, and Enteromorpha Link, 1820,
(Chlorophyceae) in the Netherlands. 201p. (Doctoral Thesis. University of Groeningen). Available at:<http://dissertations.ub.rug.nl/faculties/science/1985/r.p.t.koeman/> Access on: 25 Sep. 2014.
KUMAR, C.S.; GANESAN, P.; SURESH, P.V.; BHASKAR, N. 2008 Seaweeds as a source of nutritionally beneficial compounds. A Review. Journal of Food Science and Technology-Mysore,
45(1): 1-13.
MACCHIAVELLO, J.; BULBOA, C. 2014 Nutrient uptake efficiency of Gracilaria chilensis and Ulva
lactuca in an IMTA system with the red abalone Haliotis rufescens. Latin American Journal of
Aquatic Research, 42(3): 523-533.
MARINHO-SORIANO, E.; NUNES, S.O.; CARNEIRO, M.A.A.; PEREIRA, D.C. 2009 Nutrients removal
from aquaculture wastewater using the macroalgae Gracilaria birdiae. Biomass and Bioenergy, 33(2): 327-331.
MARINHO-SORIANO, E.; AZEVEDO, C.A.A.; TRIGUEIRO, T.G.; PEREIRA, D.C.; CARNEIRO,
M.A.A.; CAMARA, M.R. 2011 Bioremediation of aquaculture wastewater using macroalgae
and Artemia. International Biodeterioration & Biodegradation, 65(1): 253-257.
MARINHO, G.; NUNES C.; SOUSA-PINTO, I.;PEREIRA, R.; REMA, P.; VALENTE, L.M.P. 2013 The IMTA-cultivated Chlorophyta Ulva spp. as a sustainable ingredient in Nile tilapia (Oreochromis
niloticus) diets. Journal of Applied Phycology, 25(5): 1359-1367.
MARTINS, C.I.M.; EDING, E.H.; VERRETH, J.A.J. 2011 Stressing fish in Recirculating Aquaculture
Systems (RAS): does stress induced in one group of fish affect the feeding motivation of other fish
sharing the same RAS? Aquaculture Research,42(9): 1378-1384.
MARTINS, C.I.M.; EDING, E.H.; VERDEGEM, M.C.J.; HEINSBROEK, L.T.N.; SCHNEIDER, O.;
BLANCHETON, J.P.; ROQUE D’ORBCASTEL, E.; VERRETH, J.A.J. 2010 New developments in
recirculating aquaculture systems in Europe: A perspective on environmental sustainability.
Aquacultural Engineering, 43(3): 83-93.
MOURA, C.W.N. 2010 Ulvophyceae. In: FORZZA, R.C. Catálogo de plantas e fungos do Brasil. Vol. 1.
Rio de Janeiro: Andrea Jakobsson Estúdio,Instituto de Pesquisas Jardim Botí¢nico do Rio de Janeiro. p.438-448.
NEORI, A. 2008 Essential role of seaweed cultivation in integrated multi-trophic aquaculture farms
for global expansion of mariculture: an analysis.Journal of Applied Phycology, 20(5): 567í 570.
NEORI, A.; MSUYA, F.E.; SHAULI, L.;SCHUENHOFF, A.; KOPEL, F.; SHPIGEL, M.A. 2003 A novel three stage seaweed (Ulva lactuca) biofilter design for integrated mariculture. Journal of Applied Phycology, 15(6): 543í 553.
NIELSEN, M.M.; BRUHN, A.; RASMUSSEN, M.B.; OLESEN, B.; LARSEN, M.M.; MOLLER, H.B.
2012 Cultivation of Ulva lactuca with manure for simultaneous bioremediation and biomass
production. Journal of Applied Phycology, 24(3):449-458.
OLIVEIRA, V.P.; FREIRE, F.A.M.; MARINHOSORIANO, E. 2012 Influence of depth on the growth of the seaweed Gracilaria birdiae (Rhodophyta) in a shrimp pond. Brazilian Journal of Aquatic Science and Technology, 16(1): 33-39.
PEREIRA, R.; VALENTE, L.M.P.; SOUSA-PINTO, I.; REMA, P. 2012 Apparent nutrient digestibility of
seaweeds by rainbow trout (Oncorhynchus mykiss) and Nile tilapia (Oreochromis niloticus).
Algal Research, 1(1): 77-82.
PLASTINO, E.M. and OLIVEIRA, E.C. 2002 Gracilaria birdiae (Gracilariales, Rhodophyta), a new species from the tropical South American Atlantic with terete frond and deep spermatangial
conceptacles. Phycologia, 41(4): 389-396.
RAPOSO, D.; OLIVEIRA, S.R.; AFONSO, F.; FERNANDES, F.O.; MARINHO-SORIANO, E. 2014 Performance of shrimp Litopenaeus vannamei and seaweeds Gracilaria birdiae and Ulva fasciata
in an integrated multi-trophic aquaculture system. In: AQUACULTURE EUROPE, Trondheim, 2014. Anais... Trondheim: European Aquaculture Society.
ROSENTHAL, H.; CASTELL, J.D.; CHIBA, K.; FORSTER, J.R.M.; HILGE, V.; HOGENDOORN,H.; MAYO, R.D.; MUIR, J.F.; MURRAY, K.R.; PETIT, J.; WEDEMEYER, G.A.; WHEATON, F.;WICKINS, J. 1986 Flow-through and recirculation systems. EIFAC. 100p.
SODE, S.; BRUHN, A.; BALSBY, T.J.; LARSEN, M.M.; GOTFREDSEN,A.; RASMUSSEN, M.B.2013 Bioremediation of reject water anaerobically digested waste water sludge with macroalgae (Ulva lactuca, Chlorophyta).Bioresource Technology 146: 426-435.
VANDERMEULEN, H. and GORDIM, H. 1990 Ammonium uptake using Ulva (Chlorophyta) in
intensive fishpond systems: mass culture and treatment of effluent. Journal of Applied Phycology
2(4): 363-374.
VERDEGEM, M.C.J.; BOSMA, R.H.; VERRETH, J.A.J. 2005 Reducing water use for animal production
through aquaculture. International Journal of Water Resources Development, 22(1): 101-113.
YOKOYAMA, H. and ISHIHI, Y. 2010 Bioindicator and biofilter function of Ulva spp. (Chlorophyta)
for dissolved inorganic nitrogen discharged from a coastal fish farm - potential role in integrated
multi-trophic aquaculture. Aquaculture, 310(1-2): 74-83.
ZAR, J.H. 1996 Biostatistical analysis. New York:Prentice Hall, Upper Saddle River. 662p.
ZOHAR, Y.; TAL, Y.; SCHREIER, H.J.; STEVEN, C.;STUBBLEFIELD, J.; PLACE, A. 2005 Commercially
feasible urban recirculated aquaculture: addressing the marine sector. In: COSTA-PIERCE, B. Urban Aquaculture. Cambridge: CABI Publishing.p.159í 171.
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