Abstract
Seaweeds are a promising biomass resource that contain proteins with high potential for sustainable exploration. Palmaria palmata, one of the main red seaweeds of the Canadian coast, has a high protein content and much interest as an ingredient. Understanding the associations between environmental conditions and P. palmata color and chemical composition is of paramount importance to predict optimum harvesting conditions and thus increase its value. This study investigated the influence of environmental conditions on the composition and color of wild and cultivated P. palmata. Important changes in these parameters were found for P. palmata harvested in the subarctic Canadian transition zone, depending on the harvesting site/month. A marked increase in carbohydrates and decrease in ashes content (up to 2-fold) were observed from June to October, while photosynthetically active radiation (PAR) values have decreased. These associations suggest that wild P. palmata is shade acclimated to the Gulf of Saint Lawrence region. Maximum protein content was found for samples in June and was especially higher for samples from Grande-Rivière. Samples were intensely colored in June, possibly related to the higher protein content found in this month. Although several intricate factors seem to influence color development in this species, data from this study assist harvesting sites and period to maximise dark red color and avoid pigmentation degradation and paleness. In sum, these results may help indicate the best site/period to take commercial advantage of this species and orient future research on the multifactored relationships between environmental factors and macroalgae chemical composition and color.
Similar content being viewed by others
Data availability
Data available in a publicly accessible repository that does not issue DOIs Publicly available datasets were analyzed in this study. This data can be found here: [OGSL 2017 Observatoire Global du Saint-Laurence. Prévisions océaniques. https://ogsl.ca/ocean/ Accessed 15 April 2017, as described in the Methods section].
References
Adey WH, Hayek LAC (2011) Elucidating marine biogeography with macrophytes: quantitative analysis of the North Atlantic supports the thermogeographic model and demonstrates a distinct subarctic region in the Northwestern Atlantic. Northeast Nat 18:1–128
Adey WH, Lindstrom SC, Hommersand MH, Müller KM (2008) The biogeographic origin of arctic endemic seaweeds: A thermogeographic view. J Phycol 44:1384–1394
Ahmad RS, Imran A, Hussain MB (2018) Nutritional composition of meat. In: Arshad MS (ed) Meat science and nutrition. IntechOpen, London, pp 61–77
AOAC (2002) Official Methods of Analysis, 17th edn. Association of Official Analytical Chemists, Washington
Archambault P, Snelgrove PVR, Fisher JAD, Gagnon JM, Garbary DJ, Harvey M, Kenchington EL, Lesage V, Levesque M, Lovejoy C, Mickas DL, McKindsey CW, Nelson JR, Pepin P, Piche L, Poulin M (2010) From sea to sea: Canada’s three oceans of biodiversity. PLoS One 5:e12182
Badmus UO, Taggart MA, Elbourne P, Sterik HP, Boyd KG (2022) Effect of long-term storage and harvest site on the fatty acid profiles, mineral and antioxidant properties of selected edible Scottish seaweeds. Food Chem 377:131955
Barbier M, Charrier B, Araújo R, Holdt SL, Jacquemin B, Rebours C (2019) PEGASUS - phycomorph european guidelines for a sustainable aquaculture of seaweeds COST action FA1406. 1–194. https://doi.org/10.21411/2c3w-yc73
Beaulieu L, Sirois M, Tamigneaux É (2016) Evaluation of the in vitro biological activity of protein hydrolysates of the edible red alga, Palmaria palmata (dulse) harvested from the Gaspe coast and cultivated in tanks. J Appl Phycol 28:3101–3115
Bizzaro G, Vatland AK, Pampanin DM (2022) The One-Health approach in seaweed food production. Environ Int 158:106948
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
Blikra MJ, Altintzoglou T, Løvdal T, Rognså G, Skipnes D, Skåra T, Sivertsvik M, Noriega Fernández E (2021) Seaweed products for the future: Using current tools to develop a sustainable food industry. Trends Food Sci Technol 118:765–776
Britton CM, Dodd JD (1976) Relationships of photosynthetically active radiation and shortwave irradiance. Agric Meteorol 17:1–7
Castelo Pereira D, Gaban Trigueiro T, Colepicolo P, Marinho-Soriano E (2012) Seasonal changes in the pigment composition of natural population of Gracilaria domingensis (Gracilariales, Rhodophyta). Braz J Pharmacogn 22:874–880
Chinnadurai S, Kalyanasundaram G, Chermapandi P, Annadurai H, Perumal A (2013) Estimation of major pigment content in seaweeds collected from Pondicherry coast. The Experiment 9:522–525
Chopin T, Bastarache S (2004) Mariculture in Canada: finfish, shellfish and seaweed. World Aquac 35:37–41
Chopin T, Ugarte R (2006) The seaweed resources of eastern Canada. In: Critchley AT, Ohno M, Largo DB (eds) World Seaweed Resources. An Authoritative Reference System. ETI BioInformatics Publishers, Amsterdam, pp 1–46
Cox S, Gupta S, Abu-Ghannam N (2011) Application of response surface methodology to study the influence of hydrothermal processing on phytochemical constituents of the Irish edible brown seaweed Himanthalia elongata. Bot Mar 54:471–480
Davison IR, Dudgeon SR, Ruan H-M (1989) Effect of freezing on seaweed photosynthesis. Mar Ecol Prog Ser 58:123–131
Dawczynski C, Schubert R, Jahreis G (2007) Amino acids, fatty acids, and dietary fibre in edible seaweed products. Food Chem 103:891–899
de Jesus Raposo MF, de Morais AMMB, de Morais RMSC (2016) Emergent sources of prebiotics: Seaweeds and microalgae. Mar Drugs 14:27
Demetropoulos CL, Langdon CJ (2004) Enhanced 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
Drinkwater KF, Gilbert D (2004) Hydrographic variability in the waters of the Gulf of St. Lawrence, the Scotian Shelf and the eastern Gulf of Maine (NAFO Subarea 4) during 1991-2000. J Northwest Atl Fish Sci 34:85–101
Faes VA, Viejo RM (2003) Structure and dynamics of a population of Palmaria palmata (Rhodophyta) in Northern Spain. J Phycol 39:1038–1049
FAO (2016) The State of World Fisheries and Aquaculture 2016. Contributing to food security and nutrition for all. FAO, Rome
FAO (2018) The State of World Fisheries and Aquaculture 2018 - Meeting the sustainable development goals. FAO, Rome
FAO (2020) The state of World Fisheries and Aquaculture 2020. Sustainability in action. FAO, Rome
Fleurence J, Morançais M, Dumay J (2018) Seaweed proteins. In: Yada RY (ed) Proteins in food processing, second edn. Woodhead Publ, Duxford, pp 245–262
Fradette P, Bourget E, Fradette P, Bburget E (1980) Ecology of benthic epifauna of the estuary and gulf of st. lawrence: factors influencing their distribution and abundance on buoys. Can J Fish Aquat Sci 979–999
Francezon N, Tremblay A, Mouget JL, Pasetto P, Beaulieu L (2021) Algae as a source of natural flavors in innovative foods. J Agric Food Chem 69:11753–11772
Furuta T, Miyabe Y, Yasui H, Kinoshita Y, Kishimura H (2016) Angiotensin I-converting enzyme inhibitory peptides derived from phycobiliproteins of dulse Palmaria palmata. Mar Drugs 14:32
Galbraith PS, Chassé J, Gilbert D, Larouche P, Caverhill C, Lefaivre D, Brickman D, Pettigrew B, Devine L, Lafleur C (2014) Physical oceanographic conditions in the gulf of St. Lawrence in 2013. DFO Can Sci Advis Sec Res Doc 2014/062. vi + 84 p
Galland-Irmouli A-V, Fleurence J, Lamghari R, Luçon M, Rouxel C, Olivier B, Bronowicki JP, Villaume C, Guéant JL (1999) Nutritional value of proteins from edible seaweed Palmaria palmata (Dulse). J Nutr Biochem 10:353–359
Garbary DJ, Beveridge LF, Flynn AD, White KL (2012) Population ecology of Palmaria palmata (Palmariales, Rhodophyta) from harvested and non-harvested shores on Digby Neck, Nova Scotia, Canada. Algae 27:33–42
Geada P, Moreira C, Silva M, Nunes R, Madureira L, Rocha CMR, Pereira RN, Vicente AA, Teixeira JA (2021) Algal proteins: production strategies and nutritional and functional properties. Bioresour Technol 332:125125
Glazer AN, Hixson CS (1975) Characterization of R-phycocyanin. Chromophore content of R-phycocyanin and C-phycoerythrin. J Biol Chem 250:5487–5495
Guschina IA (2013) Algal lipids and their metabolism. In: Borowitzka MA, Moheimani NR (eds) Algae for Biofuels and Energy. Springer, Dordrecht, pp 17–36
Hop H, Wiencke C, Vögele B, Kovaltchouk NA (2012) Species composition, zonation, and biomass of marine benthic macroalgae in Kongsfjorden, Svalbard. Bot Mar 55:399–414
Ito K, Hori K (1989) Seaweed: chemical composition and potential food uses. Food Rev Int 5(1):101–144
Jiménez-Escrig AB, Sánchez-Muniz FJ (2000) Dietary fiber from edible seaweeds: Chemical struture, physicochemical properties and effects on cholesterol metabolism. Nutr Res 20:585–598
Kelble CR, Ortner PB, Hitchcock GL, Boyer JN (2005) Attenuation of Photosynthetically Available Radiation (PAR) in Florida Bay: potential for light limitation of primary producers. Estuaries 28:560–571
Khotimchenko SV, Yakovleva IM (2005) Lipid composition of the red alga Tichocarpus crinitus exposed to different levels of photon irradiance. Phytochemistry 66:73–79
Knudsen B, Johansen HN, Glitse V (1997) Methods for analysis of dietary fibre-advantage and limitations. J Anim Feed Sci 6:185–206
Kohata S, Matsunaga N, Hamabe Y, Hamabe K, Yumihara K, Sumi T (2010) Note Photo-stability of mixture of violet pigments phycoerythrin and phycocyanin extracted without separation from discolored nori seaweed. Food Sci Technol Res 16:617–650
Kraan S (2012) Algal polysaccharides, novel applications and outlook. In: Chang C-F (ed) Carbohydrates - comprehensive studies on glycobiology and glycotechnology. InTech, Riejeka, pp 489–532
Krogdahl Å, Jaramillo-Torres A, Ahlstrøm Ø, Chikwati E, Aasen IM, Kortner TM (2021) Protein value and health aspects of the seaweeds Saccharina latissima and Palmaria palmata evaluated with mink as model for monogastric animals. Anim Feed Sci Technol 276:114902
Lahaye M, Michel C, Luc Barry J (1993) Chemical, physicochemical and in-vitro fermentation characteristics of dietary fibres from Palmaria palmata (L.) Kuntze. Food Chem 47:29–36
Lalegerie F, Lajili S, Bedoux G, Tauphin L, Stiger-Pouvreau V, Connan S (2019) Photo-protective compounds in red macroalgae from Brittany: Considerable diversity in mycosporine-like amino acids (MAAs). Mar Environ Res 147:37–48
Larouche P, Pettigrew B (2003) Oceanographic buoy network in the Gulf of St. Lawrence. AZMP Bull 3:42–45
Lee D, Nishizawa M, Shimizu Y, Saeki H (2017) Anti-inflammatory effects of dulse (Palmaria palmata) resulting from the simultaneous water-extraction of phycobiliproteins and chlorophyll a. Food Res Int 100:514–521
Li-Beisson Y, Nakamura Y, Harwood J (2016) Lipids: From chemical structures, biosynthesis, and analyses to industrial applications. In: Nakamura Y, Li-Beisson Y (eds) Lipids in Plant and Algae Development. Subcellular Biochemistry. Springer, Cham, pp 1–18
Lourenço SO, Barbarino E, De-Paula JC, Otávio L, Pereira S, Lanfer Marquez UM (2002) Amino acid composition, protein content and calculation of nitrogen-to-protein conversion factors for 19 tropical seaweeds. Phycol Res 50:233–241
MacArtain P, Gill CIR, Brooks M, Campbell R, Rowland IR (2007) Nutritional value of edible seaweeds. Nutr Rev 65:535–543
Marson GV, de Castro RJS, Belleville M-P, Hubinger MD (2020) Spent brewer’s yeast as a source of high added value molecules: a systematic review on its characteristics, processing and potential applications. World J Microbiol Biotechnol 36:3–22
Martínez B, Rico JM (2002) Seasonal variation of P content and major N pools in Palmaria palmata (Rhodophyta). J Phycol 38:1082–1089
Martínez B, Rico JM (2008) Changes in nutrient content of Palmaria palmata in response to variable light and upwelling in Northern Spain. J Phycol 44:50–59
McHugh DJ (2003) A guide to the seaweed industry. FAO Fisheries Technical Paper 441. Food and Agriculture Organization of the United Nations, Rome, Italy
Merrill AL, Watt BK (1973) Energy value of foods: basis and derivation. USDA, Agriculture Handbook 74:1–109
Mišurcová L, Kráčmar S, Klejdus B, Vacek J (2010) Nitrogen content, dietary fiber, and digestibility in algal food products. Czech J Food Sci 28:27–35
Morgan KC, Simpson FJ (1981) The cultivation of Palmaria palmata. Effect of light intensity and temperature on growth and chemical composition. Bot Mar 24:547–552
Morgan KC, Wright JLC, Simpson FJ (1980) Review of chemical constituents of the red alga Palmaria palmata (Dulse). Econ Bot 34:27–50
Mouritsen OG, Dawczynski C, Duelund L, Jahreis G, Vetter W, Schröder M (2013) On the human consumption of the red seaweed dulse (Palmaria palmata (L.) Weber & Mohr). J Appl Phycol 25:1777–1791
Nieke B, Reuter R, Heuermann R, Wang H, Babin M, Therriault JC (1997) Light absorption and fluorescence properties of chromophoric dissolved organic matter (CDOM), in the St. Lawrence Estuary (Case 2 waters). Cont Shelf Res 17:235–252
Observatoire Global du Saint-Laurence (2017) Prévisions océaniques. https://ogsl.ca/ocean/. Accessed 12 Oct 2021
Pakker H, Martins RST, Boelen P, Buma AGJ, Nikaido O, Breeman AM (2000) Effects of temperature on the photoreactivation of ultraviolet-B–induced DNA damage in Palmaria palmata (Rhodophyta). J Phycol 36:334–341
Pang S, Lüning K (2004) Tank cultivation of the red alga Palmaria palmata: Effects of intermittent light on growth rate, yield and growth kinetics. J Appl Phycol 16:93–99
Pangestuti R, Kim SK (2011) Biological activities and health benefit effects of natural pigments derived from marine algae. J Funct Foods 3:255–266
Parjikolaei BR, Kloster L, Bruhn A, Ramussen MB, Fretté XC, Christensen KV (2013) Effect of light quality and nitrogen availability on the biomass production and pigment content of Palmaria palmata (Rhodophyta). Chem Eng Trans 32:967–972
Pighin D, Pazos A, Chamorro V, Paschetta F, Cunzolo S, Godoy F, Messina V, Pordomingo A, Grigioni G (2016) A Contribution of beef to human health: A Review of the role of the animal production systems. Sci World J 2016. https://doi.org/10.1155/2016/8681491
Qin P, Wang T, Luo Y (2022) A review on plant-based proteins from soybean: Health benefits and soy product development. J Agric Food Res 7:265
Ramus J (1983) A physiological test of the theory of complementary chromatic adaptation. II. Brown, green and red seaweeds. J Phycol 19:173–178
Ramus J, Beale ST, Mauzerall D, Howard KL (1976) Changes in photosynthetic pigment concentration in seaweeds as a function of water depth. Mar Biol 37:223–229
Rødde RSH, Vå KM, Larsen BA, Myklestad SM (2004) Seasonal and geographical variation in the chemical composition of the red alga Palmaria palmata (L.). Bot Mar 47:125–133
Rosenberg G, Ramus J (1982) Ecological growth strategies in the seaweeds Gracilaria foliifera (Rhodophyceae) and Ulva sp. (Chlorophyceae): Soluble nitrogen and reserve carbohydrates. Mar Biol 66:251–259
Sagert S, Schubert H (2000) Acclimation of Palmaria Palmata (Rhodophyta) to light intensity: Comparison between artificial and natural light fields. J Phycol 36:1119–1128
Saucier FJ, Roy F, Gilbert D, Pellerin P, Ritchie H (2003) Modeling the formation and circulation processes of water masses and sea ice in the Gulf of St. Lawrence, Canada. J Geophys Res: Ocean 108:3269
Saunders GW, Hommersand MH (2004) Assessing red algal supraordinal diversity and taxonomy in the context of contemporary systematic data. Am J Bot 91:1494–1507
Schmid M, Guihéneuf F, Nitschke U, Stengel DB (2021) Acclimation potential and biochemical response of four temperate macroalgae to light and future seasonal temperature scenarios. Algal Res 54:102190
Sharp GJ, Ugarte R, Semple R (2006) Ecological impact of marine plant harvesting in the northwest Atlantic: a review. Sci Asia 32:77–86
Soto-Sierra L, Stoykova P, Nikolov ZL (2018) Extraction and fractionation of microalgae-based protein products. Algal Res 36:175–192
Talarico L, Maranzana G (2000) Light and adaptive responses in red macroalgae: an overview. J Photochem Photobiol B 56:1–11
Tremblay A, Beaulieu L (2021) Extraction technologies for proteins and peptides. In: Rajauria G, Yuan YV (eds) Recent advances in micro and macroalgal processing: food and health perspective. John Wiley & Sons, Hoboken, pp 141–162
Vaugelade P, Hoebler C, Bernard F, Guillon F, Lahaye M, Duee PH, Darcy-Vrillon B (2000) Non-starch polysaccharides extracted from seaweed can modulate intestinal absorption of glucose and insulin response in the pig. Reprod Nutr Dev 40:33–47
Vu CHT, Won K (2014) Leaching-resistant carrageenan-based colorimetric oxygen indicator films for intelligent food packaging. J Agric Food Chem 62:7263–7267
Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, Smith AG, Camire ME, Brawley SH (2017) Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol 29:949–982
Yadav K, Reetu VS, Rai MP (2022) Algal physiology and cultivation. In: El-Sheekh M, Abomohra AE (eds) Handbook of algal biofuels. Elsevier, Amsterdam, pp 79–96
Pettigrew B, Gilbert D, Desmarais R (2017) Thermograph network in the Gulf of St. Lawrence: 2014-2016 update. Can Tech Rep Hydrogr Ocean Sci 317:54. https://publications.gc.ca/collections/collection_2017/mpo-dfo/Fs97-18-317-eng.pdf. Accessed 02/06/2022
Acknowledgments
Our thanks to the Merinov team, Marie Lionard, Isabelle Gendron-Lemieux, Lisandre Solomon and Francine Aucoin for field sample collection. The authors wish to thank Diane Gagnon (Department of Food Sciences, Laval University, QC, Canada) for her technical expertise. The authors would also like to thank the Institute of Nutrition and Functional Foods (INAF, QC, Canada), and the Fonds de Recherche Nature and Technologies (FRQNT, QC, Canada), for their financial support.
Funding
This research was funded by the Fonds de Recherche du Québec Nature et Technologies (Quebec Fund for Research in Nature and Technology), Program: “Projets de recherche en équipe”, grant number 119723.
Author information
Authors and Affiliations
Contributions
Conceptualization, M.M.M.V., E.T., S.L.T. and L.B.; methodology, M.M.M.V. and G.V.M.; validation, G.V.M., S.L.T., E.T., L.B.; formal analysis, M.M.M.V. and G.V.M.; investigation, M.M.M.V. and G.V.M.; resources, L.B.; writ-ing—original draft preparation, M.M.M.V. and G.V.M.; writing—review and editing, G.V.M., S.L.T., E.T. and L.B.; visualization, M.M.M.V. and G.V.M.; supervision, L.B.; project administration, L.B.; funding acquisition, L.B. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Vasconcelos, M.M.M., Marson, G.V., Turgeon, S.L. et al. Environmental conditions influence on the physicochemical properties of wild and cultivated Palmaria palmata in the Canadian Atlantic shore. J Appl Phycol 34, 2565–2578 (2022). https://doi.org/10.1007/s10811-022-02783-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-022-02783-2