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http://dx.doi.org/10.4490/algae.2018.33.2.21

Intensive land-based production of red and green macroalgae for human consumption in the Pacific Northwest: an evaluation of seasonal growth, yield, nutritional composition, and contaminant levels  

Gadberry, Bradley A. (Environmental and Fisheries Sciences, Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA)
Colt, John (Environmental and Fisheries Sciences, Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA)
Maynard, Desmond (Environmental and Fisheries Sciences, Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA)
Boratyn, Diane C. (Sol-Sea Ltd.)
Webb, Ken (Environmental and Fisheries Sciences, Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA)
Johnson, Ronald B. (Environmental and Fisheries Sciences, Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA)
Saunders, Gary W. (Centre for Environmental and Molecular Algal Research, Department of Biology, University of New Brunswick)
Boyer, Richard H. (Environmental and Fisheries Sciences, Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA)
Publication Information
ALGAE / v.33, no.1, 2018 , pp. 109-125 More about this Journal
Abstract
Turkish towel (Chondracanthus exasperatus), Pacific dulse (Palmaria mollis, also known as Red ribbon seaweed), and sea lettuce (Ulva spp.) were cultivated in a land-based intensive culture system at the Manchester Research Station, USA from August 2013 to September 2014. Macroalgae were grown in tumble-aerated tanks, harvested bimonthly for seasonal growth calculations, and analyzed for protein, lipid, ash, and amino acid content. Growth rate of all three species exhibited a similar pattern, with the highest specific growth rates occurring during the summer months (Turkish towel: 7.8%, Pacific dulse: 8.2%, and sea lettuce: 6.2%). Growth of all three species was lowest around winter solstice; with negative growth only observed in sea lettuce. On a dry weight basis significant differences in protein content existed between the three species with highest values for sea lettuce ($29.5{\pm}1.4%$). Lipid content varied between species (0.95-2.78%) with significantly higher lipid observed in sea lettuce (0.58-4.82%). No significant differences were detected on a seasonal basis among each species. Essential amino acids accounted for $43{\pm}0.9$ to $47{\pm}1.2%$ of total amino acids with Turkish towel having the highest value. Turkish towel had a significantly higher taurine level ($0.82{\pm}0.27$) than the other macroalgae. The levels of persistent organic pollutants and heavy metals were low. The estimated annual product of the three species ranged from 50- to $70-mt\;dry\;weight\;ha^{-1}\;y^{-1}$, significantly higher than conventional crops. Land-based culture of these species can produce year-round harvest, consistent product quality, and low contaminant levels.
Keywords
contaminants; land-based culture; macroalgae; proximate composition;
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1 Pereira, R., Yarish, C. & Critchley, A. T. 2013. Seaweed aquaculture for human foods in land-based and IMTA systems. In Christou, P. (Ed.) Sustainable Food Production. Springer Science, New York, pp. 1405-1424.
2 Polat, S. & Ozogul, Y. 2013. Seasonal proximate and fatty acid variations of some seaweeds from the northeastern Mediterranean coast. Oceanologia 55:375-391.   DOI
3 Rautenberger, R., Fernandez, P. A., Strittmatter, M., Heesch, S., Cornwall, C. E., Hurd, C. L. & Roleda, M. Y. 2015. Saturating light and not increased carbon dioxide under ocean acidification drives photosynthesis and growth in Ulva rigida (Chlorophyta). Ecol. Evol. 5:874-888.   DOI
4 Rebours, C., Marinho-Soriano, E., Zertuche-Gonzalez, J. A., Hayashi, L., Vasquez, J. A., Kradolfer, P., Soriano, G., Ugarte, R., Abreu, M. H., Bay-Larsen, I., Hovelsrud, G., Rodven, R. & Robledo, D. 2014. Seaweeds: an opportunity for wealth and sustainable livelihood for coastal communities. J. Appl. Phycol. 26:1939-1951.   DOI
5 Renaud, S. M. & Luong-Van, J. T. 2006. Seasonal variation in the chemical composition of tropical Australian marine macroalgae. J. Appl. Phycol. 18:381-387.   DOI
6 Robertson-Andersson, D. V., Potgieter, M., Hansen, J., Bolton, J. J., Troell, M., Anderson, R. J., Halling, C. & Probyn, T. 2008. Integrated seaweed cultivation on an abalone farm in South Africa. J. Appl. Phycol. 20:579-595.   DOI
7 Rosen, G., Langdon, C. J. & Evans, F. 2000. The nutritional value of Palmaria mollis cultured under different light intensities and water exchange rates for juvenile red abalone Haliotis refescens. Aquaculture 185:121-136.   DOI
8 Saunders, G. W. & Kucera, H. 2010. An evaluation of rbcL, tufA, UPA, LSU and ITS as DNA barcode markers for the marine green macroalgae. Cryptogam. Algol. 31:487-528.
9 Sloan, C. A., Anulacion, B. F., Baugh, K. A., Bolton, J. L., Boyd, D., Boyer, R. H., Burrows, D. G., Herman, D. P., Pearce, R. W. & Ylitalo, G. M. 2014. Northwest Fisheries Science Center's analyses of tissue, sediment, and water samples for organic contaminants by gas chromatography/mass spectrometry and analyses of tissue for lipid classes by thin layer chromatography/flame ionization detection. NOAA Technical Memorandum NMFS-NWFSC-125. U.S. Department of Commerce, Rockville, MD, 61 pp.
10 Saunders, G. W. & Moore, T. E. 2013. Refinements for the amplification and sequencing of red algal DNA barcode and RedToL phylogenetic markers: a summary of current primers, profiles and strategies. Algae 28:31-43.   DOI
11 Sloan, C. A., Brown, D. W., Ylitalo, G. M., Buzitis, J., Herman, D. P., Burrows, D. G., Yanagida, K., Pearce, R. W., Bolton, J. L., Boyer, R. H. & Krahn, M. M. 2006. Quality assurance plan for analyses of environmental samples for polycyclic aromatic compounds, persistent organic pollutants, fatty acids, stable isotope ratios, lipid classes, and metabolites of polycyclic aromatic compounds. NOAA Technical Memorandum NMFS-NWFSC-77. U.S. Department of Commerce, Rockville, MD, 30 pp.
12 Smith, J. L., Summers, G. & Wong, R. 2010. Nutrient and heavy metal content of edible seaweeds in New Zealand. N. Z. J. Crop. Hortic. Sci. 38:19-28.   DOI
13 Timeanddate.com. 2014. Seattle, Washington, USA: sunrise, sunset, and daylength. Available from: http://www.timeanddate.com/sun/usa/seattle. Accessed Aug 14, 2014.
14 United States Department of Agriculture. 2016. Crop Production 2015 Summary. Available from: http://www.usda.gov/nass/PUBS/TODAYRPT/cropan16.pdf. Accessed Jun 1, 2016.
15 Saunders, G. W. & McDevit, D. C. 2012. Methods for DNA barcoding photosynthetic protists emphasizing the macroalgae and diatoms. Methods Mol. Biol. 858:207-222.
16 Demetropoulos, C. L. & Langdon, C. J. 2004a. Enhance production of Pacific dulse (Palmaria mollis) for co-culture with abalone in a land-based system: effects of stocking density, light, salinity, and temperature. Aquaculture 235:471-488.   DOI
17 Waaland, J. R. 2004. Integrating intensive aquaculture of the red seaweed Chondracanthus exasperatus. Bull. Fish. Res. Agency Suppl. 1:91-100.
18 Walkiw, O. & Douglas, D. E. 1975. Health food supplements prepared from kelp: a source of elevated urinary arsenic. Clin. Toxicol. 8:325-331.   DOI
19 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
20 Abreu, M. H., Varela, D. A., Henríquez, L., Villarroel, A., Yarish, C., Sousa-Pinto, I. & Buschmann, A. H. 2009. Traditional vs. integrated multi-trophic aquaculture of Gracilaria chilensis C. J. Bird, J. McLachlan and E. C. Oliveira: productivity and physiological performance. Aquaculture 293:211-220.   DOI
21 Demetropoulos, C. L. & Langdon, C. J. 2004b. Enhanced production of Pacific dulse (Palmaria mollis) for co-culture with abalone in a land-based system: nitrogen, phosphorus, and trace metal nutrition. Aquaculture 235:433-455.   DOI
22 Department of Ecology, Marine Water Monitoring. 2017. Long-term marine water quality data. Available from:https://fortress.wa.gov/ecy/eap/marinewq/mwdataset.asp? staID=129. Accessed Dec 10, 2017.
23 Fleurence, J. 1999. Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends Food Sci. Technol. 10:25-28.   DOI
24 Fleurence, J., Gutbier, G., Mabeau, S. & Leray, C. 1994. Fatty acids from 11 marine macroalgae of the French Brittany coast. J. Appl. Phycol. 6:527-532.   DOI
25 Fleurence, J., Massiani, L., Guyader, O. & Mabeau, S. 1995. Use of enzymatic cell wall degradation for improvement of protein extraction from Chondrus crispus, Gracilaria verrucosa and Palmaria palmata. J. Appl. Phycol. 7:393-395.   DOI
26 Food and Agriculture Organization of the United Nations. 2003. Food energy: methods of analysis and conversion factors. Food and Nutrition Paper 77. Food and Agricultural Organization of the United Nations, Rome, 93 pp.
27 Food and Agriculture Organization of the United Nations. 2014. The state of world fisheries and aquaculture 2014. Food and Agriculture Organization of the United Nations, Rome, 88 pp.
28 Fortes, M. D. & Luning, K. 1980. Growth rates of North Sea macroalgae in relation to temperature, irradiance and photoperiod. Helgol. Meeresunters. 34:15-29.   DOI
29 Williams, L. G. & Krueger, C. 1988. Health risk assessment of chemical contamination in Puget Sound seafood. Prepared for U.S. Environmental Protection Agency, Region 10. PB-89-200240/XAB, Tetra Tech Inc., Bellevue,WA, 704 pp.
30 Werner, A. & Dring, M. 2011. Aquaculture explained, No. 27. Cultivating Palmaria palmata. Irish Sea FisheriesBoard, Dublin, 74 pp.
31 Yong, Y. S., Yong, W. T. L. & Anton, A. 2013. Analysis of formulae for determination of seaweed growth rate. J. Appl. Phycol. 25:1831-1834.   DOI
32 Bidwell, R. G. S., McLachlan, J. & Lloyd, N. D. H. 1985. Tank cultivation of Irish moss, Chondrus crispus Stackh. Bot. Mar. 28:87-97.
33 Aitken, K. A., Melton, L. D. & Brown, M. T. 1991. Seasonal protein variation in the New Zealand seaweeds Porphyra columbina Mont. & Porphyra subtumens J. Ag. (Rhodophyceae). Jpn. J. Phycol. 39:307-317.
34 AOAC International. 2005. Official methods of analysis of AOAC International. 18th ed. AOAC International, Gaithersburg, MD, 1298 pp.
35 Benjama, O. & Masniyom, P. 2011. Nutritional composition and physiochemical properties of two green seaweeds (Ulva pertusa and U. intestinalis) from the Pattani Bay in Southern Thailand. Songklanakarin J. Sci. Technol. 33:575-583.
36 Bolton, J. J., Robertson-Andersson, D. V., Shuuluka, D. & Kandjengo, L. 2009. Growing Ulva (Chlorophyta) in integrated systems as a commercial crop for abalone feed in South Africa: a SWOT analysis. J. Appl. Phycol. 21:575-583.   DOI
37 Gupta, S., Cox, S. & Abu-Ghannam, N. 2011. Effects of different drying temperatures on the moisture and phytochemical constituents of edible Irish brown seaweed. Food Sci. Technol. 44:1266-1272.
38 Buschmann, A. H., Mora, O. A., Gomez, P., Bottger, M., Buitano, S., Retamales, C., Vergara, P. A. & Gutierrez, A. 1994. Gracilaria chilensis outdoor tank cultivation in Chile: use of land-based salmon culture effluents. Aquac. Eng. 13:283-300.   DOI
39 Galland-Irmouli, A. V., Fleurence, J., Lamghari, R., Lucon, M., Rouxel, C., Barbaroux, O., Bronowicki, J. P., Villaume, C. & Gueant, J. L. 1999. Nutritional value of proteins from edible seaweed Palmaria palmata (dulse). J. Nutr. Biochem. 10:353-359.   DOI
40 Guillard, R. R. L. & Ryther, J. H. 1962. Studies on marine plankton diatoms: I. Cyclothella nana Huntedt andDetonula confercacae (Cleve) Gran. Can. J. Microbiol. 8:229-239.   DOI
41 Huguenin, J. E. 1976. An examination of problems and potentials for future large-scale intensive seaweed culture systems. Aquaculture 9:313-342.   DOI
42 Khairy, H. M. & El-Shafay, S. M. 2013. Seasonal variations in the biochemical composition of some common seaweed species from the coast of Abu Qir Bay, Alexandria, Egypt. Oceanologia 55:435-452.   DOI
43 Kim, J. K. & Yarish, C. 2014. Development of a sustainable land-based Gracilaria cultivation system. Algae 29:217-225.   DOI
44 Lourenco, S. O., Barbarino, E., De-Paula, J. C., Pereira, L. O. & Lanfer Marquez, U. M. 2002. Amino acid composition, protein content and calculation of nitrogen-to-protein conversion factors for 19 tropical seaweeds. Phycol. Res. 50:233-241.   DOI
45 Cornish, M. L. & Garbary, D. J. 2010. Antioxidants from macroalgae: potential applications in human health and nutrition. Algae 25:155-171.   DOI
46 Chan, J. C. -C., Cheung, P. C. -K. & Ang, P. O. 1997. Comparative studies on the effect of three drying methods on the nutritional composition of seaweed Sargassum hemiphyllum (Turn.) C. Ag. J. Agric. Food Chem. 45:3056-3059.   DOI
47 Chew, C. M. 1996. Toxicity and exposure concerns related to arsenic in seafoods: an arsenic literature review for risk assessments. U.S. Environmental Protection Agency, Region 10. EPA 910-R-96-019. ICF Kaiser, Seattle, WA, 70 pp.
48 Corey, P., Kim, J. K., Duston, J. & Garbary, D. J. 2014. Growth and nutrient uptake by Palmaria palmata integrated with Atlantic halibut in a land-based aquaculture system. Algae 29:35-45.   DOI
49 Craigie, J. S. & Shacklock, P. F. 1995. Culture of Irish moss. In Bogen, A. D. (Ed.) Cold-water Aquaculture in Atlantic Canada. 2nd ed. Canadian Institute for Research on Regional Development, Moncton, pp. 365-390.
50 Davison, A. V. & Piedrahita, R. H. 2015. Temperature modeling of a land-based aquaculture system for the production of Gracilaria pacifica: possible system modifications to conserve heat and extend the growing season. Aquac. Eng. 66:1-10.   DOI
51 Dawczynski, C., Schuert, R. & Jahreis, G. 2007. Amino acid, fatty acid, and dietary fibre in edible seaweed products. Food Chem. 103:891-899.   DOI
52 McCusker, S., Buff, P. R., Yu, Z. & Fascetti, A. J. 2014. Amino acid content of selected plant, algae and insect species: a search for alternative protein sources for use in pet foods. J. Nutr. Sci. 3:e39.
53 Lourenco, S. O., Barbarino, E., Lanfer Marquez, U. M. & Aidar, E. 1998. Distribution of intracellular nitrogen inmarine microalgae: basis for the calculation of specific nitrogen-to-protein conversion factors. J. Phycol. 34:798-811.   DOI
54 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
55 Maehre, H. K., Malde, M. K., Eilersten, K. E. & Elvevoll, E. O. 2014. Characterization of protein, lipid and mineral contents in common Norwegian seaweeds and evaluation of their potential as food and feed. J. Sci. Food Agric. 94:3281-3290.   DOI
56 Mariotti, F., Tome, D. & Mirand, P. P. 2008. Converting nitrogen into protein: beyond 6.25 and Jones' factors. Crit. Rev. Food Sci. 48:177-184.   DOI
57 Maynard, D. J., Flagg, T. A., McAuley, W. C., Frost, D. A., Kluver, B., Wastel, M. R., Colt, J. E. & Dickhoff, W. W. 2012. Fish culture technology and practices for captive broodstock rearing of ESA-listed salmon stocks. NOAA Technical Memorandum NMFS-NWFSC-117. National Marine Fisheries Service, Seattle, WA, 65 pp.
58 McHugh, D. J. 2003. A guide to the seaweed industry. FAO Fisheries Technical Paper 441. Food and Agriculture Organization of the United Nations, Rome, 105 pp.
59 Nelson, M. M., Phleger, C. F. & Nichols, P. D. 2002. Seasonal lipid composition in macroalgae of the Northeastern Pacific ocean. Bot. Mar. 45:58-65.
60 Morgan, K. C., Wright, J. L. C. & Simpson, F. J. 1980. Review of chemical constituents of the red alga Palmaria palmata (dulse). Econ. Bot. 34:27-50.   DOI
61 Neori, A., Ragg, N. L. C. & Shpigel, M. 1998. The integrated culture of seaweed, abalone, fish and clams in modular intensive land-based systems: II. Performance and nitrogen partitioning within an abalone (Haliotis tuberculata) and macroalgae culture system. Aquac. Eng. 17:215-239.   DOI
62 Pang, S. & Luning, K. 2004. Tank cultivation of the red algae Palmaria palmata: effects of intermittent light ongrowth rate, yield and growth kinetics. J. App. Phycol. 16:93-99.   DOI