Nitrogen allocation of Gracilaria tikvahiae grown in urbanized estuaries of Long Island Sound and New York City, USA: a preliminary evaluation of ocean farmed Gracilaria for alternative fish feeds
Nitrogen allocation of Gracilaria tikvahiae grown in urbanized estuaries of Long Island Sound and New York City, USA: a preliminary evaluation of ocean farmed Gracilaria for alternative fish feeds
ALGAE. 2014. Sep, 29(3): 227-235
Copyright © 2014, The Korean Society of Phycology
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
  • Received : May 01, 2014
  • Accepted : August 21, 2014
  • Published : September 15, 2014
Export by style
Cited by
About the Authors
Ronald B., Johnson
Resource Enhancement and Utilization Technologies Division, Northwest Fisheries Science Center, National Marine Fisheries Service, 2725 Montlake Blvd. E, Seattle, WA 98112, USA
Jang K., Kim
Department of Marine Sciences, University of Connecticut, One University Place, Stamford, CT 06901, USA
Lisa C., Armbruster
Resource Enhancement and Utilization Technologies Division, Northwest Fisheries Science Center, National Marine Fisheries Service, 2725 Montlake Blvd. E, Seattle, WA 98112, USA
Charles, Yarish
Department of Ecology and Evolutionary Biology, University of Connecticut, One University Place, Stamford, CT 06901, USA

The red seaweed, Gracilaria tikvahiae McLachlan, was cultivated in open water farms in urbanized estuaries of Long Island Sound (26-30 psu of salinity) and New York City (20-25 psu), USA in 2011. Plants were harvested monthly from summer (August, 24℃) to fall (November, 13℃) and analyzed for total nitrogen, protein, and amino acid content. On a dry matter (DM) basis, nitrogen and protein significantly increased over the harvest period until October and then plateaued. Nitrogen increased from 22 ± 1 g kg -1 DM in August to 39 ± 3 g kg -1 DM in October (p < 0.001). Protein increased from 107 ± 13 g kg -1 DM in August to 196 ± 5 g kg -1 DM in November (p < 0.001). With two exceptions, amino acid concentrations expressed on a crude protein (CP) basis were similar over the harvest period. Essential amino acids accounted for 48 ± 1% of all amino acids present with lysine and methionine averaging 56 ± 2 g kg -1 CP and 18 ± 1 g kg -1 CP, respectively. Histidine was underrepresented among essential amino acids and averaged 13 ± 1 g kg -1 CP. Taurine ranged from 2.1 to 3.2 g kg -1 DM. With its moderate levels of lysine, methionine and taurine, ocean farmed G. tikvahiae has the potential of overcoming many nutrient deficiencies currently associated with terrestrial plant ingredients in alternative feeds for fish and shrimp.
Aquaculture is the fastest growing food producing sector in the world today, and demands for feed ingredients, especially fish meal and oil, have increased dramatically in recent years ( Hardy et al. 2001 , National Research Council 2011 , Food and Agriculture Organization of the United Nations 2014 ). Macroalgae have successfully been incorporated into fish and shrimp feeds at levels up to approximately 100 g kg -1 feed without compromising growth or survival ( Mustafa et al. 1995 , Valente et al. 2006 , Khan et al. 2008 , Ergün et al. 2009 ). Occasionally, increases in feed consumption and growth have been reported. Red sea bream Pagrus major growth improved with a 50 g kg -1 addition of the green alga Ulva pertusa , the brown alga Ascophyllum nodosum , or the red alga Pyropia yezoensis (see AlgaeBase for authorities; Guiry and Guiry 2014 ) to the feed, although the largest weight gain was observed with the red alga ( Mustafa et al. 1995 ). Ergün et al. (2009) reported an increase in the growth of Nile tilapia Oreochromis niloticus when Ulva rigida was added at a level of 50 g kg -1 feed while Stadtlander et al. (2013) reported an increase in growth in tilapia when P. yezoensis was added at 136 g kg -1 , but not when added at 272 g kg -1 .
Gracilaria and related genera comprise about 200 species of warm water to tropical seaweeds that are widely distributed throughout the world, except the polar seas ( McLachlan and Bird 1984 , Lüning 1990 , Yang et al. 2012 , Guiry and Guiry 2014 ). Gracilaria is a bushy, branching seaweed, irregularly or dichotomously branched, and may have rounded, compressed, or flattened axes ( Lüning 1990 ). Blades are usually red, but can be brownish, green, or almost black depending on light and nutrient conditions (Kim and Yarish submitted). Gracilaria has a wide range of tolerance to nutrients, salinity, and temperature ( Lüning 1990 , Yokoya et al. 1999 , Choi et al. 2006 , Thomsen and McGlathery 2007 ). The genus is common to estuaries and bays and is often found in intertidal or shallow subtidal areas, less than 1 m deep, either attached to rocks or free floating. It is also found in embayments that may be rich in inorganic nitrogen and phosphorus (~55 μmol L -1 of nitrogen and ~19 μmol L -1 of phosphorus) ( Hanisak 1990 , Yarish et al. 1991 , Teichberg et al. 2008 , Kim et al. 2014 ). The native Gracilaria tikvahiae and its invasive congener Gracilaria vermiculophylla are commonly found along the northeastern United States coastline and the two are virtually indistinguishable, except by genetic markers ( Saunders 2009 , Kim et al. 2010 , Nettleton et al. 2013 ). G. tikvahiae is a euryhaline species, which can tolerate a wide range of salinities, 15-60 psu, though it grows best from 15-38 psu ( Bird and McLachlan 1986 ). It can survive temperatures of 10-30℃ but has an optimal range of 20-25℃ ( Bird et al. 1979 , McLachlan and Bird 1984 ).
At present, the annual global harvest of Gracilaria is about 1.7 million metric tons with an annual value of $540 million USD ( Yang and Yarish 2011 ). Gracilaria has historically been a commercial source of food grade and biotechnological grade agar, and its economic value is very stable ( Yarish and Pereira 2008 ). Beyond its traditional uses, Gracilaria may be suitable for biofuel production ( Notoya 2010 ), an ingredient for fish feeds ( Mustafa and Nakagawa 1995 , Kanjana et al. 2011 , Fleurence et al. 2012 ) and employed for nutrient bioextraction in integrated multi-trophic aquaculture (IMTA) systems ( Abreu et al. 2009 , 2011 , 2011 , 2011 , Yarish and Kim 2013 , Kim et al. 2014 ).
In the present study, we cultivated native G. tikvahiae in open water farms in urbanized estuaries of Long Island Sound and the Bronx River, New York, USA to extract nutrients from these urbanized estuaries and potentially produce a valuable ingredient for aquaculture feeds. The study sites are located within the Long Island Sound watershed and New York City’s estuary, which receive anthropogenic inputs from a population of 9 million people ( Latimer et al. 2014 ). It was previously demonstrated that G. tikvahiae readily sequesters nitrogen and carbon from these sites ( Kim et al. 2014 ). However, it is unknown how much sequestered nitrogen is present as protein and how nutritious this protein is for aquaculture species. As such, the objective of this study was to determine the protein and amino acid composition of G. tikvahiae harvested from these nutrient bioextraction systems over a four month harvest period and evaluate the potential of this algal protein as an ingredient for fish and shrimp feeds.
- Algae culture
A G. tikvahiae strain (G-RI-ST 1 ) was mass cultured at the Seaweed Marine Biotechnology Laboratory at University of Connecticut, Stamford, CT, USA. This strain was originally collected in June 2010 from Potters Pond, South Kingstown, Rhode Island, USA (41°22′56″ N, 71°32′04″ W). G. tikvahiae was out-planted on long lines at two open water farm sites, 67 km apart. The first out-planting was on July 28, 2011 in Long Island Sound (LIS; 41°4′8″ N, 73°9′10″ W), and the second out-planting was on September 20, 2011 at the mouth of the Bronx River Estuary (BRE; 40°48′5″ N, 73°52′16″ W). For each site, long lines (45 m at the BRE site and 100 m at the LIS site) were installed at 0.5 m depth as described elsewhere ( Kim et al. 2014 ). Twenty gram bundles of G. tikvahiae thalli were inserted into nylon rope line for both sites. Three bundles were harvested on Aug 16, Sep 15, and Nov 4, 2011 from the LIS site and on Oct 19, 2011 from the BRE site for tissue analysis.
Salinity during the growing season at LIS ranged from 26-30 psu, and at BRE were slightly lower, 20-25 psu. Subsurface irradiance was measured with a LiCor LI-185A PAR meter (Lincoln, NE, USA) as described elsewhere ( Kim et al. 2014 ). At the LIS site, mean light penetration was 81% at 0.5 m and 53% at 1.0 m deep, during mid-day on cloudless days. Mean light penetration at the BRE site was similar to the LIS site at 81% at 0.5 m and 48% at 1.0 m deep. The water temperature at both sites and at the culture depth ranged 22-24℃ (July to September) and decreased to 13℃ by early November ( Kim et al. 2014 ). Seawater nitrogen and phosphorus content was monitored at the two sites through the automated determination of total ammonia (Bertheot method), nitrate + nitrate (cadmium reduction, azo dye method), and dissolved inorganic phosphorus (acidified molybdate method) on a QuAAtro Autoanalyzer (Seal Analytical, Mequon, WI, USA) as described by Hansen and Koroleff (1999). Nitrogen concentrations at the LIS site ranged 2.7-8.4 μmol L -1 while those at the BRE site were 38-55 μmol L -1 during the 2011 summer-fall growing season. Phosphorus concentrations during the same time period ranged 0.9-4.7 μmol L -1 at the LIS site and 14-19 μmol L -1 at the BRE site.
- Nutrient analysis
Approximately 100 g of G. tikvahiae from different clean bundles, without fouling organisms, were sampled for nutrient analysis at each harvest (n = 3). Samples were immediately dried at 55℃ and stored in a dry environment until shipment. The dried samples were shipped to the Northwest Fisheries Science Center, Seattle, WA, USA for protein extraction and constituent analyses. Upon receipt, algal samples were dried overnight in a 105℃ oven to a constant weight and then finely ground. Protein was extracted via precipitation with 5% trichloroacetic acid (TCA) as described by Woyewoda et al. (1986) . Dried algae and TCA protein extracts were finely ground and sent to the University of Missouri Agriculture Experiment Station Chemical Laboratory, Columbia, MO, USA for Kjeldahl nitrogen analyses in accordance with AOAC Official Method 984.13 ( AOAC International 2000 ). Dried algal samples were additionally analyzed for complete amino acid profiles in accordance with AOAC Official Method 982.30 ( AOAC International 2000 ).
Total nitrogen and crude protein (CP) are expressed on a dry matter (DM) basis of the original algal sample. In accordance with AOAC methodology, the CP content of algae was estimated by multiplying protein nitrogen by a factor of 6.25. For comparative purposes, amino acid concentrations are presented both on a DM basis and a CP basis.
- Statistical analysis
All statistical analyses were performed with R version 2.15.0 statistical software (The R Foundation for Statistical Computing, Palo Alto, CA, USA). One-way analysis of variance (ANOVA) was employed to detect differences in total nitrogen and protein over time with differences between means detected by Tukey’s HSD test. Differences in nitrogen content attributable to harvest date were deemed significant when p < 0.05.
One-way ANOVA was similarly employed to detect differences in amino acid concentrations on a CP basis over time with differences between means detected by Tukey’s honestly significant difference test. After applying the Bonferroni correction for multiple comparisons (n = 19) at the p < 0.05 level, differences in amino acid concentrations attributable to harvest date were deemed significant when p < 0.0026. Unless stated otherwise, results are presented as mean ± standard deviation.
- Nitrogen and protein content ofGracilaria tikvahiae
Total nitrogen and protein nitrogen increased proportionately over the harvest period ( Fig. 1 ). On average, non-protein nitrogen (NPN) accounted for 21 ± 1% of all nitrogen present. Total nitrogen increased from 22 ± 1 g kg -1 DM in August to 39 ± 3 g kg -1 DM in October (p < 0.001), with no difference observed between October and November (p = 0.90). CP followed a similar trend and increased from 107 ± 13 g kg -1 DM in August to 196 ± 5 g kg -1 DM in November (p < 0.001) with no difference observed between October and November (p = 0.45).
PPT Slide
Lager Image
Increases in total and protein nitrogen of Gracilaria tikvahiae harvested from Long Island Sound (LIS) and the Bronx River Estuary (BRE), New York, USA during Summer and Fall 2011. August 16, September 15, and November 4 harvests were at the LIS site. October 19 harvest was at the BRE site. Values are mean ± standard deviation, n = 3, except for protein nitrogen at the BRE site where n = 2.
- TauAmino acid and taurine content ofGracilaria tikvahiae
Increases in amino acids mirrored that of CP ( Table 1 ). The two most abundant amino acids at all harvests were aspartic acid and glutamic acid with mean concentrations of 102 ± 3 g kg -1 CP and 101 ± 5 g kg -1 CP, respectively. With two exceptions, amino acid concentrations expressed on a CP basis were similar over time. Tryptophan significantly increased from 6.3 ± 0.3 CP g kg -1 in August to 8.9 ± 0.9 g kg -1 CP in October (p = 0.002) with no differences observed between October and November. Conversely, cysteine significantly decreased from 30 ± 1 g kg -1 CP in August to 24 ± 2 g kg -1 CP in September (p = 0.002) and remained at this lower concentration through November.
Amino acid composition of protein extracted fromGracilaria tikvahiaeharvested from Long Island Sound (LIS) and the Bronx River Estuary (BRE), New York, USA
PPT Slide
Lager Image
Values are the mean concentration on a dry matter basis (g kg-1 DM) and crude protein basis in parentheses (g kg-1 CP) (n = 3). a,bFor a particular amino acid, concentrations with different lowercase letters are significantly different on a CP basis (p < 0.0026). cn = 2 for CP values.
Over the harvest period, essential amino acids accounted for 48 ± 1% of all amino acids present. Lysine and methionine were present at moderate concentrations, averaging 56 ± 2 g kg -1 CP and 18 ± 1 g kg -1 CP, respectively. Histidine was underrepresented among essential amino acids and averaged 13 ± 1 g kg -1 CP. Taurine concentrations ranged from 2.1 to 3.2 g kg -1 DM.
The nitrogen content of G. tikvahiae grown at our study sites ranged from 22-39 g kg -1 DM. This is similar to levels previously reported for Gracilaria species collected from the wild ( Bird et al. 1977 , Penniman et al. 1986 , Lourenço et al. 2002 , Abreu et al. 2011 ), but less than levels reported from some shore-based IMTA systems ( Valente et al. 2006 , Abreu et al. 2011 ). The two-fold increase in the nitrogen content of G. tikvahiae between August to November is consistent with results from a previous study with this species raised in the Great Bay Estuary, NH, USA ( Penniman and Mathieson 1987 ) and another study with Gracilaria sp. raised in Pomquet Harbour, NS, Canada ( Bird et al. 1977 ). The increase in protein content of G. tikvahiae from 106 to 196 g kg -1 over the harvest period, suggests that ocean farmed G. tikvahiae may be a suitable ingredient for aquaculture feeds, especially when harvested late in the season.
Amino acid concentrations, expressed on a CP basis, were relatively constant during the study. This demonstrates the conserved nature of G. tikvahiae protein over the harvest period. NPN was slightly higher than NPN reported for Pyropia sp. (15% NPN) by Dawczynski et al. (2007) , but within the range (7-32% NPN) reported by Lourenço et al. (2002) for other red algal species. Compared to terrestrial grasses and legume forages routinely fed to ruminants, NPN levels in dried G. tikvahiae were higher than levels typical for fresh plants (10-15% NPN), similar to levels in hay (15-25% NPN), and lower than levels in silages (30-65% NPN) ( National Research Council 2001 ).
The two major amino acids present in G. tikvahiae at all four harvests were aspartic and glutamic acid, which accounted for over 20% of the protein present. This is similar to values reported for other red algal species ( Dawczynski et al. 2007 , Gressler et al. 2010 ), and less that what has been reported for brown algae ( Dawczynski et al. 2007 , MacArtain et al. 2007 ). Lysine was detected in moderate amounts in G. tikvahiae and unlikely to be a limiting amino acid in feed formulations. However, histidine and methionine were present at lower concentrations and may be limiting. Low concentrations of histidine were similarly observed in four Brazilian red algae species ( Gressler et al. 2010 ) and Porphyra and Pyropia spp. ( Walker et al. 2009 ). Based on the National Research Council (NRC)’s “ideal protein” profiles for fish and shrimp ( National Research Council 2011 ), histidine is likely to be the first limiting amino acid for G. tikvahiae protein in aquaculture feeds, followed by methionine ( Table 2 ). An “ideal protein” contains a perfect balance of essential amino acids for the animal. The NRC ideal protein profiles for fish and shrimp are compiled from 15 nutritional studies spanning 10 different species and are a useful starting point for formulating aquaculture feeds. In a feeding study with juvenile Atlantic cod, Walker et al. (2009) overcame the low histidine content of Porphyra and Pyropia spp. by concomitantly adding blood meal to the experimental feeds.
Ideal amino acid profiles for teleost fish and penaeid shrimp with the amino acid profile ofGracilariatikvahiaeprotein harvested from Long Island Sound and the Bronx River Estuary, New York, USA
PPT Slide
Lager Image
G. tikvahiae values are the mean ± standard error of mean, n = 4. aData from National Research Council (2011).
The lower tryptophan concentrations observed among August plants suggests that tryptophan may additionally be limiting for feeds prepared from plants harvested in the summer. Similarly, tryptophan and histidine were the first two limiting amino acids in Gracilaria domingensis for red hake Urophycis chuss followed by methionine and lysine ( Burkholder et al. 1971 ). By comparison, tryptophan in P. yezoensis protein was below levels required by tilapia, despite observing an increase in growth when 15% of the fish meal in their experimental feeds was replaced by P. yezoensis ( Stadtlander et al. 2013 ).
Taurine in G. tikvahiae , 1.3-2.1% of the amino acids present, was slightly lower than values reported for Pyropia produced in Japan, but similar to levels reported for Pyropia produced in China ( Dawczynski et al. 2007 ). Taurine levels of G. tikvahiae exceeded those previously reported for brown algae ( Dawczynski et al. 2007 ). Taurine, an amino sulfonic acid, has important roles in osmoregulation, bile acid conjugation, membrane stabilization and calcium homeostasis in vertebrates ( Huxtable 1992 ). The capacity of cultured fish to biosynthesize taurine depends on the species, with marine species typically unable to biosynthesize enough taurine for optimum growth. Although the underlying physiological processes are not yet understood, the addition of taurine to the diet can improve the growth of important marine aquaculture species such as olive flounder Paralichthys olivaceus ( Kim et al. 2005 ), red sea bream ( Matsunari et al. 2008 ), and cobia Rachycentron canadum ( Lunger et al. 2007 ) as well as some freshwater species such as rainbow trout Oncorhynchus mykiss ( Gaylord et al. 2006 ). While ample amounts of taurine are found in many animal proteins, including fish meal, taurine is absent from terrestrial plants. However, taurine is present in macroalgae, which makes them an attractive ingredient for alternative, plant based, aquaculture feeds ( Pedersen et al. 2012 ).
Farming macroalgae is an economical way to remove nutrients from eutrophic coastal waters and waters around finfish farms ( White et al. 2011 , Kim et al. 2013 , Corey et al. 2014 ). It was estimated that G. tikvahiae cultured in this study removed as much as 94 kg nitrogen ha -1 and 727 kg carbon ha -1 from the BRE site over a 90-day growing period ( Kim et al. 2014 ). Algae raised in areas contaminated by anthropogenic activities; however, may additionally sequester persistent toxins present in the environment ( Cheney et al. 2007 , Cruz-Uribe et al. 2007 , Lotufo et al. 2008 ). While the presence of persistent organic pollutants is typically low in algae, high levels of heavy metals in some species have raised concerns regarding the use of algae for human food and animal feeds ( Almela et al. 2002 , Besada et al. 2009 , Yokoi and Konomi 2012 ). Concern heightens when algae are harvested from areas historically contaminated from industrial activity ( Giusti 2001 , Lotufo et al. 2008 , Lorenzana et al. 2009 ). Because of these concerns, we are currently measuring the concentration and seasonal variability of heavy metals in G. tikvahiae harvested at the two study sites and will be presenting these results in a future article. Initial results indicate that algae harvested at the two sites will not exceed the US Food and Drug Administrations’ regulatory limits for arsenic, cadmium, mercury, and lead for animal feeds.
In conclusion, results from this preliminary study suggest that ocean farmed G. tikvahiae may be a suitable protein ingredient for aquaculture feeds, especially when harvested late in the season. With its moderate levels of lysine, methionine and taurine, G. tikvahiae has the potential of overcoming many nutrient deficiencies currently associated with terrestrial plant proteins presently used in alternative fish feeds. In addition, since macroalgae do not require fresh water for growth, their culture may be more economical and environmentally sustainable for some regions of the world than terrestrial plants.
This study was supported by grants to C. Yarish from Connecticut Sea Grant College Program (Grant # RA/38) and EPA Long Island Sound Futures Fund grants from the National Fish and Wildlife Foundation (Legacy Grant Project ID: 1401.10.024266). We thank Dr. Shannon Meseck (NOAA Fisheries, Northeast Fisheries Science Center, Milford, Connecticut, USA) for the seawater analyses.
Abreu M. H. , Pereira R. , Buschmann A. H. , Sousa-Pinto I. , Yarish C. 2011 Nitrogen uptake responses of Gracilaria vermiculophylla (Ohmi) Papenfuss under combined and single addition of nitrate and ammonium J. Exp. Mar. Biol. Ecol. 407 190 - 199    DOI : 10.1016/j.jembe.2011.06.034
Abreu M. H. , Pereira R. , Sousa-Pinto I. , Yarish C. 2011 Ecophysiological studies of the non-indigenous species Gracilaria vermiculophylla (Rhodophyta) and its abundance patterns in Ria de Aveiro Lagoon Portugal Eur. J. Phycol. 46 453 - 464    DOI : 10.1080/09670262.2011.633174
Abreu M. H. , Pereira R. , Yarish C. , Buschmann A. H. , Sousa-Pinto I. 2011 IMTA with Gracilaria vermiculophylla: productivity and nutrient removal performance of the seaweed in a land-based pilot scale system Aquaculture 312 77 - 87    DOI : 10.1016/j.aquaculture.2010.12.036
Abreu M. H. , Varela D. A. , Henríquez L. , Villarroel A. , Yarish C. , Sousa-Pinto I. , Buschmann A. H. 2009 Oliveira: productivity and physiological performance Aquaculture 293 211 - 220    DOI : 10.1016/j.aquaculture.2009.03.043
Almela C. , Algora S. , Benito V. , Clemente M. J. , Devesa V. , Súñer M. A. , Vélez D. , Montoro R. 2002 Heavy metal total arsenic and inorganic arsenic contents of algae food products J. Agric. Food Chem. 50 918 - 923    DOI : 10.1021/jf0110250
Horwitz W. 2000 Official Methods of Analysis of AOAC International AOAC International Arlington, VA
Besada V. , Andrade J. M. , Schultze F. , González J. J. 2009 Heavy metals in edible seaweeds commercialised for human consumption J. Mar. Syst. 75 305 - 313    DOI : 10.1016/j.jmarsys.2008.10.010
Bird C. J. , Edelstein T. , McLachlan J. 1977 Studies on Gracilaria Experimental observations on growth and reproduction in Pomquet Harbour Nova Scotia Nat. can. 104 245 - 255
Bird C. J. , McLachlan J. 1986 The effect of salinity on distribution of species Gracilaria Grev (Rhodophyta Gigartinales): an experimental assessment Bot. Mar. 29 231 - 238
Bird N. L. , Chen L. C. -M. , McLachlan J. 1979 Effects of temperature light and salinity on growth in culture of Chondrus crispus Furcellaria lumbricalis Gracilaria tikvahiae (Gigartinales Rhodophyta) and Fucus serratus (Fucales Phaeophyta) Bot. Mar. 22 521 - 527
Burkholder P. R. , Burkholder L. M. , Almodovar L. R. 1971 Nutritive constiuents of some Caribbean marine algae Bot. Mar. 14 132 - 135
Cheney D. , Brudner M. , Aulisio D. , Gardner K. 2007 Seaweed removal and remediation of organic pollutants from marine sediments Eur. J. Phycol. 44 80 - 81
Choi H. G. , Kim Y. S. , Kim J. H. , Lee S. J. , Park E. J. , Ryu J. , Nam K. W. 2006 Effects of temperature and salinity on the growth of Gracilaria verrucosa and G chorda with the potential for mariculture in Korea J. Appl. Phycol. 18 269 - 277    DOI : 10.1007/s10811-006-9033-y
Corey Peter , Kim Jang K. , Duston Jim , Garbary David J. 2014 Growth and nutrient uptake by Palmaria palmata integrated with Atlantic halibut in a land-based aquaculture system Algae 29 (1) 35 - 45    DOI : 10.4490/algae.2014.29.1.035
Cruz-Uribe O. , Cheney D. P. , Rorrer G. L. 2007 Comparison of TNT removal from seawater by three marine macroalgae Chemosphere 67 1469 - 1476    DOI : 10.1016/j.chemosphere.2007.01.001
Dawczynski C. , Schubert R. , Jahreis G 2007 Amino acids, fatty acids, and dietary fibre in edible seaweed products Food Chem 103 891 - 899    DOI : 10.1016/j.foodchem.2006.09.041
Ergün S. , Soyutürk M. , Güroy B. , Güroy D. , Merrifield D. 2009 Influence of Ulva meal on growth feed utilization and body composition of juvenile Nile tilapia (Oreochromis niloticus) at two levels of dietary lipid Aquac. Int. 17 355 - 361    DOI : 10.1007/s10499-008-9207-5
Fleurence J. , Morançais M. , Dumay J. , Decottignies P. , Turpin V. , Munier M. , Garcia-Bueno N. , Jaouen P. 2012 What are the prospects for using seaweed in human nutrition and for marine animals raised through aquaculture? Trends Food Sci. Technol. 27 57 - 61    DOI : 10.1016/j.tifs.2012.03.004
2014 The state of the world fisheries and aquaculture FAO Fisheries and Aquaculture Department Rome 202 -
Gaylord T. G. , Teague A. M. , Barrows F. T. 2006 Taurine supplementation of all-plant protein diets for rainbow trout (Oncorhynchus mykiss) J. World Aquac. Soc. 37 509 - 517    DOI : 10.1111/j.1749-7345.2006.00064.x
Giusti L. 2001 Heavy metal contamination of brown seaweed and sediments from the UK coastline between the Wear river and the Tees river Environ. Int. 26 275 - 286    DOI : 10.1016/S0160-4120(00)00117-3
Gressler V. , Yokoya N. S. , Fujii M. T. , Colepicolo P. , Filho J. M. , Torres R. P. , Pinto E 2010 Lipid, fatty acid, protein, amino acid and ash contents in four Brazilian red algae species Food Chem 120 585 - 590    DOI : 10.1016/j.foodchem.2009.10.028
Guiry M. D. , Guiry G. M. 2014 AlgaeBase World-wide electronic publication, National University of Ireland Galway Available from:
Hanisak M. D. 1990 The use of Gracilaria tikvahiae (Gracilariales Rhodophyta) as a model system to understand the nitrogen nutrition of culture seaweeds Hydrobiologia 204/205 79 - 87    DOI : 10.1007/BF00040218
Hansen H. P. , Koroleff F. , Grasshoff K. , Cremling K. , Erhardt M. Methods of Seawater Analysis Wiley-VCH Verlag Weinheim Determination of nutrients 159 - 228
Hardy R. W. , Higgs D. , Lall S. , Tacon A. G. J. 2001 Alternative dietary protein and lipid sources for the sustainable production of salmonids Havforskningsinstituttet (Institute of Marine Research) Bergen 55 -
Huxtable R. J. 1992 Physiological actions of taurine Physiol. Rev. 72 101 - 163
Kanjana K. , Radtanatip T. , Asuvapongpatana S. , Withyachumnarnkul B. , Wongprasert K. 2011 Solvent extracts of the red seaweed Gracilaria fisheri prevent Vibrio harveyi infections in the black tiger shrimp Penaeus monodon Fish Shellfish Immunol. 30 389 - 396    DOI : 10.1016/j.fsi.2010.11.016
Khan M. N. D. , Yoshimatsu T. , Kalla A. , Araki T. , Sakamoto S. 2008 Supplemental effect of Porphyra spheroplasts on the growth and feed utilization of black sea bream Fish. Sci. 74 397 - 404    DOI : 10.1111/j.1444-2906.2008.01536.x
Kim J. K. , Duston J. , Corey P. , Garbary D. J. 2013 Marine finfish effluent bioremediation: effects of stocking density and temperature on nitrogen removal capacity of Chondrus crispus and Palmaria palmata (Rhodophyta) Aquaculture 414-415 210 - 216    DOI : 10.1016/j.aquaculture.2013.08.008
Kim J. K. , Kraemer G. P. , Yarish C. 2014 Field scale evaluation of seaweed aquaculture as a nutrient bioextraction strategy in Long Island Sound and the Bronx River Estuary Aquaculture 433 148 - 156    DOI : 10.1016/j.aquaculture.2014.05.034
Kim S. -K. , Takeuchi T. , Yokoyama M. , Murata Y. , Kaneniwa M. , Sakakura Y 2005 Effect of dietary taurine levels on growth and feeding behavior of juvenile Japanese flounder Paralichthys olivaceus Aquaculture 250 765 - 774    DOI : 10.1016/j.aquaculture.2005.04.073
Kim S. Y. , Weinberger F. , Boo S. M. 2010 Genetic data hint at a common donor region for invasive Atlantic and Pacific populations of Gracilaria vermiculophylla (Gracilariales Rhodophyta) J. Phycol. 46 1346 - 1349    DOI : 10.1111/j.1529-8817.2010.00905.x
Latimer J. S. , Tedesco M. A. , Swanson R. L. , Yarish C. , Stacey P. E. , Garza C. 2014 Long Island sound: prospects for the urban sea. Springer New York 558 -
Lorenzana R. M. , Yeow A. Y. , Colman J. T. , Chappell L. L. , Choudhury H. 2009 Arsenic in seafood: speciation issues for human health assessment Hum. Ecol. Risk Assess. 15 185 - 200    DOI : 10.1080/10807030802615949
Lotufo G. R. , Lydy M. J. , Rorrer G. , Cruz-Uribe O. , Cheney D. P. , Sunahara G. I. , Lotufo G. , Kuperman R. G. , Hawari J. 2008 Ecotoxicology of Explosives CRC Press Boca Raton, FL Bioconcentration, bioaccumulation, and biotransformation of explosives and related compounds in aquatic organisms 135 - 155
Lourenço S. O. , Barbarino E. , De-Paula J. C. , Pereira L. O. D. S. , Marquez U. M. L. 2002 Amino acid composition protein content and calculation of nitrogen-to-protein conversion factors for 19 tropical seaweeds Phycol. Res. 50 233 - 241    DOI : 10.1111/j.1440-1835.2002.tb00156.x
Lunger A. N. , McLean E. , Gaylord T. G. , Kuhn D. , Craig S. R 2007 Taurine supplementation to alternative dietary proteins used in fish meal replacement enhances growth of juvenile cobia (Rachycentron canadum) Aquaculture 271 401 - 410    DOI : 10.1016/j.aquaculture.2007.07.006
Lüning K. , Yarish C. , Kirkman H. 1990 Verbreitung, Okophysiologie und Nutzung der marinen Makroalgen by Klaus Luning John Wiley and Sons, Inc. New York Seaweeds-their environment, biogeography, and ecophysiology 1 - 527
MacArtain P. , Gill C. I. R. , Brooks M. , Campbell R. , Rowland I. R. 2007 Nutritional value of edible seaweeds Nutr. Rev. 65 535 - 543    DOI : 10.1111/j.1753-4887.2007.tb00278.x
Matsunari H. , Furuita H. , Yamamoto T. , Kim S. -K. , Sakakura Y. , Takeuchi T. 2008 Effect of dietary taurine and cystine on growth performance of juvenile red sea bream Pagrus major Aquaculture 274 142 - 147    DOI : 10.1016/j.aquaculture.2007.11.002
McLachlan J. , Bird C. J. 1984 Geographical and experimental assessment of the distribution of Gracilaria species (Rhodophyta: Gigartinales) in relation to temperature Helgol. Meeresunters. 38 319 - 334    DOI : 10.1007/BF02027684
Mustafa G. , Wakamatsu S. , Takeda T. , Umino T. , Nakagawa H. 1995 Effects of algae meal as feed additive on growth feed efficiency and body composition in red sea bream Fish. Sci. 61 25 - 28
Mustafa M. G. , Nakagawa H. 1995 A review: dietary benefits of algae as an additive in fish feed Isr. J. Aquac.-Bamidgeh 47 155 - 162
2001 Nutrient requirements of dairy cattle 7th ed National Academies Press Washington, DC 381 -
2011 Nutrient requirements of fish and shrimp National Academies Press Washington, DC 376 -
Nettleton J. C. , Mathieson A. C. , Thornber C. , Neefus C. D. , Yarish C. 2013 Introduction of Gracilaria vermiculophylla (Rhodophyta, Gracilariales) to New England, USA: estimated arrival times and current distribution Rhodora 115 28 - 41    DOI : 10.3119/12-07
Notoya M. , Isreal A. , Einav R. , Seckbach J. 2010 Seaweeds and Their Role in Globally Changing Environments Springer Dordrecht Production of biofuel by macroalgae with preservation of marine resources and environment 217 - 228
Pedersen A. , Kraemer G. , Hariskov S. , Yarish C. , Sahoo D. , Kaushik D. B. 2012 Algal Biotechnology and Environment I.K. International Publishing House New Delhi Porphyra spp. from Long Island sound: free amino acids, Tot. C, Tot. N and phycobiliproteins content and the response to short term uptake of nitrate 129 - 144
Penniman C. A. , Mathieson A. C. 1987 Variation in chemical composition of Gracilaria tikvahiae McLachlan (Gigartinales Rhodophyta) in the Great Bay Estuary New Hampshire Bot. Mar. 30 525 - 534
Penniman C. A. , Mathieson A. C. , Penniman C. E. 1986 Reproductive phenology and growth of Gracilaria tikvahiae McLachlan (Gigartinales Rhodophyta) in the Great Bay Estuary New Hampshire Bot. Mar. 29 147 - 154
Saunders G. W. 2009 Routine DNA barcoading of Canadian Gracilariales (Rhodophyta) reveals the invasive species Gracilaria vermiculophylla in British Columbia Mol. Ecol. Resour. 9 (SSuppl. 1) 140 - 150
Stadtlander T. , Khalil W. K. B. , Focken U. , Becker K. 2013 Effects of low and medium levels of red alga Nori (Porphyra yezoensis Ueda) in the diets on growth feed utilization and metabolism in intensively fed Nile tilapia Oreochromis niloticus (L) Aquac. Nutr. 19 64 - 73    DOI : 10.1111/j.1365-2095.2012.00940.x
Teichberg M. , Fox S. E. , Aguila C. , Olsen Y. S. , Valiela I. 2008 Macroalgal responses to experimental nutrient enrichment in shallow coastal waters: growth internal nutrient pools and isotopic signatures Mar. Ecol. Prog. Ser. 368 117 - 126    DOI : 10.3354/meps07564
Thomsen M. S. , McGlathery K. J. 2007 Stress tolerance of the invasive macroalgae Codium fragile and Gracilaria vermiculophylla in a soft- bottom turbid lagoon Biol. Invasions 9 499 - 513    DOI : 10.1007/s10530-006-9043-3
Valente L. M. P. , Gouveia A. , Rema P. , Matos J. , Gomes E. F. , Pinto I. S. 2006 Evaluation of three seaweeds Gracilaria bursa-pastoris Ulva rigida and Gacilaria cornea as dietary ingredients in European sea bass (Dicentrarchus labrax) juveniles Aquaculture 252 85 - 91    DOI : 10.1016/j.aquaculture.2005.11.052
Walker A. B. , Fournier H. R. , Neefus C. D. , Nardi G. C. , Berlinsky D. L. 2009 Partial replacement of fish meal with laver Porphyra spp in diets for Atlantic cod N. Am. J. Aquac. 71 39 - 45    DOI : 10.1577/A07-110.1
White Katelyn L. , Kim Jang-Kyun , Garbary David J. 2011 Effects of landbased fish farm effluent on the morphology and growth of Ascophyllum nodosum (Fucales, Phaeophyceae) in southwestern Nova Scotia Algae 26 (3) 253 - 263    DOI : 10.4490/algae.2011.26.3.253
Woyewoda A. D. , Shaw S. J. , Ke P. J. , Burns. B. G. 1986 Recommended laboratory methods for assessment of fish quality. Canadian technical report of fisheries and aquatic sciences. No. 1448 Department of Fisheries and Oceans Halifax, NS 143 -
Yang Mi-Yeon , Dong Jun-De , Kim Myung-Sook 2012 Taxonomic notes on five species of Gracilariaceae from Hainan, China Algae 27 175 - 187    DOI : 10.4490/algae.2012.27.3.175
Yang Y. , Yarish C. 2011 Gracilaria cultivation can provide bioremediation in Chinese mariculture mussel culture Glob. Aquac. Advocate 14 50 - 51
Yarish C. , Kilar J. A. , Merrill J. E. , Hinga K. R. , Stanley D. W. , Klein C. J. , Lucid D. T. , Katz M. J. , Eds. 1991 The management of eutrophication through aquaculture and natural beds of marine algae.; National Oceanic and Atmospheric Administration and the University of Rhode Island Graduate School of Oceanography Rockville, MD The National Estuarine Eutrophication Project: Workshop Proceedings Eds. 40 - 41
Yarish C. , Kim J. K. 2013 Exploring integrated multi-trophic aquaculture (IMTA) linkage through nutrient bioextraction: the use of ecological methods to integrate the cultivation of seaweeds to remediate nitrified coastal waters In Vitro Cell. Dev. Biol. Anim. 49 (Suppl. 1) 2 - 3    DOI : 10.1007/s11626-013-9615-3
Yarish C. , Pereira R. , Jorgensen S. E. , Fath B. D. 2008 Ecological Engineering Elsevier Oxford Mass production of marine macroalgae 2236 - 2247
Yokoi K. , Konomi A. 2012 Toxicity of so-called edible hijiki seaweed (Sargassum fusiforme) containing inorganic arsenic Regul. Toxicol. Pharmacol. 63 291 - 297    DOI : 10.1016/j.yrtph.2012.04.006
Yokoya N. S. , Kakita H. , Obika H. , Kitamura T. 1999 Effects of environmental factors and plant growth regulators on growth of the red algae Gracilaria vermiculophylla from Shikoku Island Japan Hydrobiologia 398/398 339 - 347