Skip to main content
Log in

Nutritional evaluation of Gracilaria pulvinata as partial substitute with fish meal in practical diets of barramundi (Lates calcarifer)

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

A 40-day feeding trial was carried out to investigate the potential of red algal (Gracilaria pulvinata) meal as a protein source in formulated diets for barramundi (Lates calcarifer) (initial mean body weight of 28.5 ± 0.5 g). Five practical diets were prepared using a fishmeal-based diet used as positive control (PC) and blends of soybean meal and fishmeal used as a negative control (NC), in which NC was supplemented with 3 (GL3%), 6 (GL6%), and 9% (GL9%) G. pulvinata. Each dietary treatment was replicated in triplicate. Results indicated that growth and feeding performance including specific growth rate, feed conversion, protein efficiency ratios, and feed intake in all treatments were not significantly different (P > 0.05). Crude protein, lipid, and ash contents of fish carcass were not markedly altered in all dietary treatments. Serum lysozyme, alternative complement activities, serum immunoglobulin, and total protein content significantly decreased in fish fed GL9 diets. Increasing dietary supplementation of G. pulvinata decreased the serum triglycerides and cholesterol when compared to the NC. Gracilaria inclusion levels did not affect intestinal total protease and amylase activities (P < 0.05); however, intestine lipase activity in fish fed GL6 diets was significantly higher than other groups (P < 0.05). The results of the present study recommend the inclusion of Gracilaria meal up to 3%, without significant negative effects on the growth performance, body composition, and health parameters of L. calcarifer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anson ML (1938) The estimation of pepsin, trypsin, papain, and cathepsin with hemoglobin. J Gen Physiol 22:79–89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • AOAC (1995) Official methods of analysis of Official Analytical Chemists International, 16th edn. Association of Official Analytical Chemists, Arlington

    Google Scholar 

  • Araújo M, Rema P, Sousa-Pinto I, Cunha LM, Peixoto MJ, Pires MA, Seixas F, Brotas V, Beltrán C, Valente LMP (2016) Dietary inclusion of IMTA-cultivated Gracilaria vermiculophylla in rainbow trout (Oncorhynchus mykiss) diets: effects on growth, intestinal morphology, tissue pigmentation, and immunological response. J Appl Phycol 28:679–689

    Article  Google Scholar 

  • Azaza MS, Mensi F, Ksouri J, Dhraief MN, Brini B, Abdelmouleh A, Kraïem MM (2008) Growth of Nile tilapia (Oreochromis niloticus L.) fed with diets containing graded levels of green algae Ulva meal (Ulva rigida) reared in geothermal waters of southern Tunisia. J Appl Ichthyol 24:202–207

    Article  CAS  Google Scholar 

  • Azodi M, Nafisi M, Morshedi V, Modarresi M, Faghih-Ahmadani A (2016) Effects of intermittent feeding on compensatory growth, feed intake and body composition in Asian sea bass (Lates calcarifer). Iran J Fish Sci 15(1):144–156

    Google Scholar 

  • Banerjee K, Mitra A, Mondal K (2010) Cost-effective and eco-friendly shrimp feed from red seaweed Catenella repens (Gigartinales: Rhodophyta). Curr Biot 4:23–43

    Google Scholar 

  • Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 1:3–26

    Article  Google Scholar 

  • Børgesen F (1939) Marine algae from the Iranian Gulf especially from the innermost part near Bushehr and Khark. In: Jessen K, Spärck R (eds) Danish scientific investigations in Iran. Part I. Munksgaard, Copenhagen, pp 47–141

    Google Scholar 

  • Blender AE (1967) Dietetic foods. Leonard Hill Books, London, p 211

    Google Scholar 

  • Boonyaratpalin M, Suraneiranat P, Tunpibal T (1998) Replacement of fishmeal with various type of soybean products in diets for Asian seabass, Lates calcarifer. Aquaculture 161:67–78

    Article  CAS  Google Scholar 

  • Boshra H, Li J, Sunyer JO (2006) Recent advances on the complement system of teleost fish. Fish Shellfish Immunol 20:239–262

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Castro IA, Barroso LP, Sinnecker P (2005) Functional foods for coronary heart disease risk reduction: a meta-analysis using a multivariate approach. Am J Clin Nutr 82:32–40

    Article  CAS  PubMed  Google Scholar 

  • Castro R, Zarra I, Lamas J (2004) Water-soluble seaweed extracts modulate the respiratory burst activity of turbot phagocytes. Aquaculture 229:67–78

    Article  Google Scholar 

  • Cheng AC, Chen YY, Chen JC (2008) Dietary administration of sodium alginate and k-carrageenan enhances the innate immune response of brown-marbled grouper Epinephelus fuscoguttatus and its resistance against Vibrio alginolyticus. Vet Immunol Immunopathol 121:206–215

    Article  CAS  PubMed  Google Scholar 

  • Chou RL, Her BY, Su MS, Hwang G, Wu YH, Chen HY (2004) Substituting fish meal with soybean meal in diets of juvenile cobia Rachycentron canadum. Aquaculture 229:325–333

    Article  Google Scholar 

  • Davis DA (2015) Feed and feeding practices in aquaculture. Woodhead Publishing, Cambridge

    Google Scholar 

  • Deng J, Mai K, Ai Q, Zhang W, Wang X, Xu W, Liufu Z (2006) Effects of replacing fish meal with soy protein concentrate on feed intake and growth of juvenile Japanese flounder, Paralichthys olivaceus. Aquaculture 258:503–513

    Article  CAS  Google Scholar 

  • Dumas BT, Watson WA, Biggs HG (1997) Albumin standards and the measurement of serum albumin with bromcresol green. 1971. Clin Chim Acta 258:21–30

    Article  CAS  PubMed  Google Scholar 

  • Dvir I, Stark AH, Chayoth R, Madar Z, Arad SM (2009) Hypocholesterolemic effects of nutraceuticals produced from the red microalga Porphyridium sp. in rats. Nutrients 1:156–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dy Peñaflorida V, Golez NV (1996) Use of seaweed meals from Kappaphycus alvarezii and Gracilaria heteroclada as binders in diets for juvenile shrimp Penaeus monodon. Aquaculture 143:393–401

    Article  Google Scholar 

  • Ellis A (1990) Lysozyme assays. In: Stolen JS, Fletcher TC, Anderson DP, Roberson BS, van Muiswinkel WB (eds) Techniques in fish immunology. SOS Publications, New Jersey, pp 101–103

    Google Scholar 

  • El-Sayed A-FM (1994) Evaluation of soybean meal, spirulina meal and chicken offal meal as protein sources for silver seabream (Rhabdosargus sarba) fingerlings. Aquaculture 127:169–176

    Article  CAS  Google Scholar 

  • FAO (2014) The State of World Fisheries and Aquaculture 2014 (SOFIA). Rome

  • FAO (2012) The State of World Fisheries and Aquaculture. Rome

  • Fevolden SE, Røed KH, Gjerde B (1994) Genetic components of post-stress cortisol and lysozyme activity in Atlantic salmon; correlations to disease resistance. Fish Shellfish Immunol 4:507–519

    Article  Google Scholar 

  • Floreto EAT, Bayer RC, Brown PB (2000) The effects of soybean-based diets, with and without amino acid supplementation, on growth and biochemical composition of juvenile American lobster, Homarus americanus. Aquaculture 189:211–235

    Article  CAS  Google Scholar 

  • Francis G, Makkar HPS, Becker K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227

    Article  CAS  Google Scholar 

  • Fujiki K, Matsuyama H, Yano T (1994) Protective effect of sodium alginates against bacterial infection in common carp, Cyprinus carpio L. J Fish Dis 17:349–355

    Article  CAS  Google Scholar 

  • Furné M, García-Gallego M, Hidalgo MC, Morales AE, Domezain A, Domezain J, Sanz A (2008) Effect of starvation and refeeding on digestive enzyme activities in sturgeon (Acipenser naccarii) and trout (Oncorhynchus mykiss). Comp Biochem Physiol A 149:420–425

    Article  Google Scholar 

  • Gabrielsen BO, Austreng E (1998) Growth, product quality and immune status of Atlantic salmon, Salmo salar L., fed wet feed with alginate. Aquac Res 29:397–401

    Article  Google Scholar 

  • Grant G, Alonso R, Edwards JE, Murray S (2000) Dietary soya beans and kidney beans stimulate secretion of cholecystokinin and pancreatic digestive enzymes in 400-day-old hooded-Lister rats but only soya beans induce growth of the pancreas. Pancreas 20:305–312

    Article  CAS  PubMed  Google Scholar 

  • Güroy B, Ergün S, Merrifield DL, Güroy D (2013) Effect of autoclaved Ulva meal on growth performance, nutrient utilization and fatty acid profile of rainbow trout, Oncorhynchus mykiss. Aquac Int 21:605–615

    Article  Google Scholar 

  • Hashim R, Saat MAM (1992) The utilization of seaweed meals as binding agents in pelleted feeds for snakehead (Channa striatus) fry and their effects on growth. Aquaculture 108:299–308

    Article  Google Scholar 

  • Jerry DR (2013) Biology and culture of Asian seabass Lates calcarifer. CRC Press

  • Kim KW, Bai SC, Koo JW, Wang X, Kim SK (2002) Effects of dietary Chlorella ellipsoidea supplementation on growth, blood characteristics, and whole-body composition in juvenile japanese flounder Paralichthys olivaceus. J World Aquac Soc 33:425–431

    Article  Google Scholar 

  • Krogdahl A, Bakke-McKellep AM, Baeverfjord G (2003) Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.) Aquac Nutr 9:361–371

    Article  Google Scholar 

  • Krogdahl Å, Lea TB, Olli JJ (1994) Soybean proteinase inhibitors affect intestinal trypsin activities and amino acid digestibilities in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol A 107:215–219

    Article  Google Scholar 

  • Kumar S, Sahoo D, Levine I (2015) Assessment of nutritional value in a brown seaweed Sargassum wightii and their seasonal variations. Algal Res 9:117–125

    Article  Google Scholar 

  • Kumar S, Sahu N, Pal A, Choudhury D, Yengkokpam S, Mukherjee S (2005) Effect of dietary carbohydrate on haematology, respiratory burst activity and histological changes in L. rohita juveniles. Fish Shellfish Immunol 19:331–344

    Article  CAS  PubMed  Google Scholar 

  • Matanjun P, Mohamed S, Muhammad K, Mustapha NM (2010) Comparison of cardiovascular protective effects of tropical seaweeds, Kappaphycus alvarezii, Caulerpa lentillifera, and Sargassum polycystum, on high-cholesterol/high-fat diet in rats. J Med Food 13:792–800

    Article  CAS  PubMed  Google Scholar 

  • Matanjun P, Mohamed S, Mustapha NM, Muhammad K (2009) Nutrient content of tropical edible seaweeds, Eucheuma cottonii, Caulerpa lentillifera and Sargassum polycystum. J Appl Phycol 21:75–80

    Article  CAS  Google Scholar 

  • Montero D, Tort L, Izquierdo MS, Robaina L, Vergara JM (1998) Depletion of serum alternative complement pathway activity in gilthead seabream caused by α-tocopherol and n-3 HUFA dietary deficiencies. Fish Physiol Biochem 18:399–407

    Article  CAS  Google Scholar 

  • Morshedi V, Kochanian P, Bahmani M, Yazdani-Sadati MA, Pourali HR, Ashouri G, Pasha-Zanoosi H, Azodi M (2013) Compensatory growth in sub-yearling Siberian sturgeon, Acipenser baerii Brandt, 1869: effects of starvation and refeeding on growth, feed utilization and body composition. J Appl Ichthyol 29:978–983

    Article  CAS  Google Scholar 

  • Mustafa GM, 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

    Article  CAS  Google Scholar 

  • Nafisi M, Soltani M (2008) Effect of different dietary energy levels and feeding rates on growth and body composition of fingerling rainbow trout, Oncorhynchus mykiss. Iran J Fish Sci 7:171–186

    Google Scholar 

  • Nakagawa H (1997) Effect of dietary algae on improvement of lipid metabolism in fish. Biomed Pharmacother 51:345–348

    Article  CAS  PubMed  Google Scholar 

  • NRC (2011) Nutrient requirements of fish and shrimp, 1st edn. National Academies Press, Washington, DC

    Google Scholar 

  • Obach A, Quentel C, Baudin Laurencin F (1993) Effects of alpha-tocopherol and dietary oxidized fish oil on the immune response of sea bass Dicentrarchus labrax. Dis Aquat Org 15:175–185

    Article  CAS  Google Scholar 

  • Oliveira MN, Ponte-Freitas AL, Urano-Carvalho AF, Taveres-Sampaio TM, Farias DF, Alves-Teixera DI, Gouveia ST, Gomes-Pereira J, Castro-Catanho de Sena MM (2009) Nutritive and non-nutritive attributes of washed-up seaweeds from the coast of Ceara. Brazil. Food Chem 11:254–259

    Article  Google Scholar 

  • Opstvedt J, Nygård E, Samuelsen TA, Venturini G, Luzzana U, Mundheim H (2003) Effect on protein digestibility of different processing conditions in the production of fish meal and fish feed. J Sci Food Agric 83:775–782

    Article  CAS  Google Scholar 

  • Peixoto MJ, Salas-Leitón E, Pereira LF, Queiroz A, Magalhães F, Pereira R, Abreu H, Reis PA, Gonçalves JFM, de Ozório ROA (2016) Role of dietary seaweed supplementation on growth performance, digestive capacity and immune and stress responsiveness in European seabass (Dicentrarchus labrax). Aquac Reports 3:189–197

    Article  Google Scholar 

  • Pereira R, Valente LMP, Sousa-Pinto I, Rema P (2012) Apparent nutrient digestibility of seaweeds by rainbow trout (Oncorhynchus mykiss) and Nile tilapia (Oreochromis niloticus). Algal Res 1:77–82

    Article  CAS  Google Scholar 

  • Ragaza JA, Koshio S, Mamauag RE, Ishikawa M, Yokoyama S, Villamor SS (2015) Dietary supplemental effects of red seaweed Eucheuma denticulatum on growth performance, carcass composition and blood chemistry of juvenile Japanese flounder, Paralichthys olivaceus. Aquac Res 46:647–657

    Article  CAS  Google Scholar 

  • Rajapakse N, Kim SK (2011) Nutritional and digestive health benefits of seaweed. Adv Food Nutr Res 64:17–28

    Article  CAS  PubMed  Google Scholar 

  • Ramnani P, Chitarrari R, Tuohy K, Grant J, Hotchkiss S, Philp K, Campbell R, Gill C, Rowland I (2012) In vitro fermentation and prebiotic potential of novel low molecular weight polysaccharides derived from agar and alginate seaweeds. Anaerobe 18:1–6

    Article  CAS  PubMed  Google Scholar 

  • Refstie S, Storebakken T, Roem AJ (1998) Feed consumption and conversion in Atlantic salmon (Salmo salar) fed diets with fish meal, extracted soybean meal or soybean meal with reduced content of oligosaccharides, trypsin inhibitors, lectins and soya antigens. Aquaculture 162:301–312

    Article  CAS  Google Scholar 

  • Saurabh S, Sahoo PK (2008) Lysozyme: an important defence molecule of fish innate immune system. Aquac Res 39:223–239

    Article  CAS  Google Scholar 

  • Shapawi R, Safiin NSZ, Senoo S (2015) Improving dietary red seaweed Kappaphycus alvarezii (Doty) Doty ex P. Silva meal utilization in Asian seabass Lates calcarifer. J Appl Phycol 27:1681–1688

    Article  CAS  Google Scholar 

  • Singh RK (2000) Growth, survival and production of Lates calcarifer in a seasonal rain-fed coastal pond of the Konkan region. Aquaculture 8:55–60

    Google Scholar 

  • Siwicki AK, Anderson DP (1993) Nonspecific defence mechanisms assay in fish II; potential killing activity of neutrophils and manocytes, lysozyme activity in serum and organs and total immunoglobulin (Ig) level in serum. In: Siwicki AK, Anderson DP, Waluga J (eds) Wydawnictwo Instytutu Rybactwa Strodladowego, Olsztyn, pp 105–111

  • Skulas-Ray AC, West SG, Davidson MH, Kris-Etherton PM (2008) Omega-3 fatty acid concentrates in the treatment of moderate hypertriglyceridemia. Expert Opin Pharmacother 9:1237–1248

    Article  CAS  PubMed  Google Scholar 

  • Sotoudeh E, Abedian Kenari A, Khodabandeh S, Khajeh K (2016a) Combination effects of dietary EPA and DHA plus alpha-tocopherol: effects on performance and physiological status of Caspian brown trout (Salmo trutta caspius) fry. Aquac Nutr 22:1101–1115

    Article  CAS  Google Scholar 

  • Sotoudeh E, Amiri Moghaddam J, Shahhosseini G, Aramli MS (2016b) Effect of dietary gamma-irradiated and fermented soybean meal on the growth performance, body composition, and digestive enzymes activity of caspian brown trout, Salmo trutta caspius, juvenile. J World Aquacult Soc 47:830–842

    Article  CAS  Google Scholar 

  • Sotoudeh E, Jafari M (2017). Effects of dietary supplementation with red seaweed, Gracilaria pygmaea, on growth, carcass composition and hematology of juvenile rainbow trout, Oncorhynchus mykiss. Aquac Int. doi:10.1007/s10499-017-0158-6

  • Southgate P, Lucas J (2012) Reproduction, life cycles and growth. In: Lucas JS, Southgate PC (eds) Aquaculture: farming aquatic animals and plants. Wiley-Blackwell Publishing Ltd, Oxford, pp 126–137

    Google Scholar 

  • Stadtlander T, Khalil WKB, 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

    Article  CAS  Google Scholar 

  • Tabarsa M, Rezaei M, Ramezanpour Z, Waaland JR (2012) Chemical compositions of the marine algae Gracilaria salicornia (Rhodophyta) and Ulva lactuca (Chlorophyta) as a potential food source. J Sci Food Agric 92:2500–2506

    Article  CAS  PubMed  Google Scholar 

  • Tantikitti C, Sangpong W, Chiavareesajja S (2005) Effects of defatted soybean protein levels on growth performance and nitrogen and phosphorus excretion in Asian seabass (Lates calcarifer). Aquaculture 248:41–50

    Article  CAS  Google Scholar 

  • Thanigaivel S, Chandrasekaran N, Mukherjee A, Thomas J (2015) Investigation of seaweed extracts as a source of treatment against bacterial fish pathogen. Aquaculture 448:82–86

    Article  Google Scholar 

  • Tort L, Gomez E, Montero D, Sunyer JO (1996) Serum haemolytic and agglutinating activity as indicators of fish immunocompetence: their suitability in stress and dietary studies. Aquac Int 4:31–41

    Article  Google Scholar 

  • Valente LMP, Araújo M, Batista S, Peixoto MJ, Sousa-Pinto I, Brotas V, Cunha LM, Rema P (2016) Carotenoid deposition, flesh quality and immunological response of Nile tilapia fed increasing levels of IMTA-cultivated Ulva spp. J Appl Phycol 28:691–701

    Article  CAS  Google Scholar 

  • Valente LMP, Gouveia A, Rema P, Matos J, Gomes EF, Pinto IS (2006) Evaluation of three seaweeds Gracilaria bursa-pastoris, Ulva rigida and Gracilaria cornea as dietary ingredients in European sea bass (Dicentrarchus labrax) juveniles. Aquaculture 252:85–91

    Article  Google Scholar 

  • Van Alstyne K, Wolfe G, Freidenburg T, Neill A, Hicken C (2001) Activated defense systems in marine macroalgae: evidence for an ecological role for DMSP cleavage. Mar Ecol Prog Ser 213:53–65

    Article  Google Scholar 

  • Van Doan H, Doolgindachbaporn S, Suksri A (2014) Effects of low molecular weight agar and Lactobacillus plantarum on growth performance, immunity, and disease resistance of basa fish (Pangasius bocourti, Sauvage 1880). Fish Shellfish Immunol 41:340–345

    Article  PubMed  Google Scholar 

  • Vizcaíno AJ, Mendes SI, Varela JL, Ruiz-Jarabo I, Rico R, Figueroa FL, Abdala R, Moriñigo MÁ, Mancera JM, Alarcón FJ (2015) Growth, tissue metabolites and digestive functionality in Sparus aurata juveniles fed different levels of macroalgae, Gracilaria cornea and Ulva rigida. Aquac Res 47:3224–3238

    Article  Google Scholar 

  • Walker AB, Fournier HR, Neefus CD, Nardi GC, Berlinsky DL (2009) Partial replacement of fish meal with laver Porphyra spp. in diets for Atlantic cod. N Am J Aquac 71:37–41

    Article  Google Scholar 

  • Wassef EA, Masry MHE, Mikhail FR (2001) Growth enhancement and muscle structure of striped mullet, Mugil cephalus L., fingerlings by feeding algal meal-based diets. Aquac Res 32:315–322

    Article  Google Scholar 

  • Wiegertjes GF, Stet RM, Parmentier HK, van Muiswinkel WB (1996) Immunogenetics of disease resistance in fish: a comparative approach. Dev Comp Immunol 20:365–381

    Article  CAS  PubMed  Google Scholar 

  • Xu S, Zhang L, Wu Q, Liu X, Wang S, You C, Li Y (2011) Evaluation of dried seaweed Gracilaria lemaneiformis as an ingredient in diets for teleost fish Siganus canaliculatus. Aquac Int 19:1007–1018

    Article  CAS  Google Scholar 

  • Xuan X, Wen X, Li S, Zhu D, Li Y (2013) Potential use of macro-algae Gracilaria lemaneiformis in diets for the black sea bream, Acanthopagrus schlegelii, juvenile. Aquaculture 412–413:167–172

    Article  Google Scholar 

  • Yano T (1996) The non-specific immune system: humoral defense. In: Iwama G, Nakanishi T (eds) The fish immune system: organism, pathogen, and environment. Academic Press, New York, pp 105–157

    Chapter  Google Scholar 

  • Yone Y, Furuichi M, Urano K (1986) Effects of wakame Undaria pinnatifida and Ascophyllum nodosum on absorption of dietary nutrients, and blood sugar and plasma free amino-N levels of red sea bream. Nippon Suisan Gakkaishi 52:1817–1819

    Article  Google Scholar 

  • Zambonino Infante JL, Cahu CL (2007) Dietary modulation of some digestive enzymes and metabolic processes in developing marine fish: applications to diet formulation. Aquaculture 268:98–105

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors express their sincere appreciation to Mr. Omid Bahri and Dr. Hadi Khaliji from Bushehr Polymer Industry Group for assisting in analysis of algae composition. This study was supported by Research Enhancement Grant of Persian Gulf University (394/07/01).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Mahmoud Nafisi Bahabadi or Ebrahim Sotoudeh.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Morshedi, V., Nafisi Bahabadi, M., Sotoudeh, E. et al. Nutritional evaluation of Gracilaria pulvinata as partial substitute with fish meal in practical diets of barramundi (Lates calcarifer). J Appl Phycol 30, 619–628 (2018). https://doi.org/10.1007/s10811-017-1199-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-017-1199-y

Keywords

Navigation