Skip to main content
SpringerLink
Log in

Inclusion of 10% seaweed meal in diets for juvenile and on-growing life stages of Senegalese sole (Solea senegalensis)

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

Abstract

The long-term inclusion of 10% seaweed meal (Ulva rigida and Undaria pinnatifida) was evaluated in diets for Senegalese sole (Solea senegalensis). Triplicate groups of fish with an initial body weight of 23 g were fed the experimental diets (ULVA and UNDARIA) and compared to fish fed a control diet with no seaweed included (CTRL), both in juvenile (after 5 months of feeding, up to 60 g) and on-growing stages (after 9 months of feeding, up to 160 g). In the early juvenile phase, the inclusion of seaweeds did not affect fish growth, but final body weight was significantly lower in on-growing fish fed the UNDARIA diet. Overall, growth performance was also reduced in fish fed the UNDARIA diet, with a significantly lower daily growth index. Whole-body composition and nutrient retention (% intake) remained unaffected by the dietary treatment, but by the end of the growth trial fish fed the UNDARIA diet had a significantly lower protein gain associated with significantly lower intestinal villi width. At the end of the experiment, fish fed the UNDARIA diet had a significantly higher iodine flesh content (375.7 μg kg−1) than those fed the CTRL (187.5 μg kg−1) or ULVA (199.3 μg kg−1) diets, whereas selenium content was similar in all groups of fish. In conclusion, U. rigida seems a valid ingredient for Senegalese sole diets without affecting fish growth or nutrient utilization. Undaria pinnatifida was an effective way of naturally fortifying the nutritional value of sole fillets for human consumption, but resulted in growth impairment, so a lower inclusion level should be further evaluated.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abdel-Warith AW, Younis el SM, Al-Asgah NA (2016) Potential use of green macroalgae Ulva lactuca as a feed supplement in diets on growth performance, feed utilization and body composition of the African catfish, Clarias gariepinus. Saudi J Biol Sci 23:404–409

    Article  Google Scholar 

  • Andreakis N, Schaffelke B (2012) Invasive marine seaweeds: pest or prize? In: Wiencke C, Bischof K (eds) Seaweed biology. Springer, Berlin pp ??

    Google Scholar 

  • AOAC (2006) Official methods of analysis of AOAC International. Maryland, USA

    Google Scholar 

  • APROMAR (2016) La acuicultura en España. Asociación Empresarial de Productores de Cultivos Marinos de España (APROMAR)

  • 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 

  • Bell JG, Henderson RJ, Tocher DR, McGhee F, Dick JR, Porter A, Smullen RP, Sargent JR (2002) Substituting fish oil with crude palm oil in the diet of Atlantic salmon (Salmo salar) affects muscle fatty acid composition and hepatic fatty acid metabolism. J Nutr 132:222–230

    Article  CAS  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  Google Scholar 

  • Borges P, Medale F, Veron V, Pires Mdos A, Dias J, Valente LM (2013) Lipid digestion, absorption and uptake in Solea senegalensis. Comp Biochem Physiol A 166:26–35

    Article  CAS  Google Scholar 

  • Borges P, Oliveira B, Casal S, Dias J, Conceicao L, Valente LM (2009) Dietary lipid level affects growth performance and nutrient utilisation of Senegalese sole (Solea senegalensis) juveniles. Br J Nutr 102:1007–1014

    Article  CAS  Google Scholar 

  • Cabral EM, Bacelar M, Batista S, Castro-Cunha M, Ozorio ROA, Valente LMP (2011) Replacement of fishmeal by increasing levels of plant protein blends in diets for Senegalese sole (Solea senegalensis) juveniles. Aquaculture 322:74–81

    Article  Google Scholar 

  • Cabral EM, Fernandes TJR, Campos SD, Castro-Cunha M, Oliveira MBPP, Cunha LM, Valente LMP (2013) Replacement of fish meal by plant protein sources up to 75% induces good growth performance without affecting flesh quality in ongrowing Senegalese sole. Aquaculture 380-383:130–138

    Article  CAS  Google Scholar 

  • Castillo-Duran C, Ruz M (2004) Epidemiology of micronutrient deficiencies in developing and developed countries, specifically zinc, copper, selenium and iodine. In: Pettifor JM, Zlotkin S (eds) Micronutrient Deficiencies during the Weaning Period and the First Years of Life. Nestlé Nutrition Workshop Series Pediatric Program, vol 54. Nestec Ltd., Vevey/S. Karger AG, Basel, pp 37–52

  • Dantagnan P, Hernández A, Borquez A, Mansilla A (2009) Inclusion of macroalgae meal (Macrocystis pyrifera) as feed ingredient for rainbow trout (Oncorhynchus mykiss): effect on flesh fatty acid composition. Aquac Res 41:87–94

    Article  CAS  Google Scholar 

  • Dawczynski C, Schubert R, Jahreis G (2007) Amino acids, fatty acids, and dietary fibre in edible seaweed products. Food Chem 103:891–899

    Article  CAS  Google Scholar 

  • Diler I, Tekinay A, Güroy D, Güroy BK, Soyutürk M (2007) Effects of Ulva rigida on the growth, feed intake and body composition of common carp, Cyprinus carpio L. J Biol Sci 7:305–308

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • FEAP (2016) European Aquaculture Production Report 2007-2015. Fed Eur Aqua Prod (FEAP)

  • Fernandes TJ, Alves RC, Souza T, Silva JM, Castro-Cunha M, Valente LM, Oliveira MB (2012) Lipid content and fatty acid profile of Senegalese sole (Solea senegalensis Kaup, 1858) juveniles as affected by feed containing different amounts of plant protein sources. Food Chem 134:1337–1342

    Article  CAS  Google Scholar 

  • Fernández-Reiriz MJ, Pérez-Camacho A, Ferreiro MJ, Blanco J, Planas M, Campos MJ, Labarta U (1989) Biomass production and variation in the biochemical profile (total protein, carbohydrates, RNA, lipids and fatty acids) of seven species of marine microalgae. Aquaculture 83:17–37

    Article  Google Scholar 

  • FishStatJ (2018) FishStatJ—software for fishery statistical time series. http://www.fao.org/fishery/. Accessed 27 February 2018

  • Fleurence J (2004) Seaweed proteins. In: Yada RY (ed) Proteins in food processing. Woodhead Publishing Limited, pp 197–211. https://doi.org/10.1533/9781855738379.1.197

    Chapter  Google Scholar 

  • Fung A, Hamid N, Lu J (2013) Fucoxanthin content and antioxidant properties of Undaria pinnatifida. Food Chem 136:1055–1062

    Article  CAS  Google Scholar 

  • Grammes F, Reveco F, Romarheim O, Landsverk T, Mydland L, Øverland M (2013) Candida utilis and Chlorella vulgaris counteract intestinal inflammation in Atlantic Salmon (Salmo salar L.). PLoS One 8:e83213

    Article  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 

  • Güroy BK, Cirik Ş, Güroy D, Sanver F, Tekinay AA (2007) Effects of Ulva rigida and Cystoseira barbata meals as a feed additive on growth performance, feed utilization,and body composition of Nile tilapia, Oreochromis niloticus. Turk J Vet Anim Sd 31:91–97

    Google Scholar 

  • Güroy D, Güroy B, Merrifield DL, Ergün S, Tekinay AA, Yigit M (2011) Effect of dietary Ulva and Spirulina on weight loss and body composition of rainbow trout, Oncorhynchus mykiss (Walbaum), during a starvation period. J Anim Physiol Anim Nutr (Berl) 95:320–327

    Article  Google Scholar 

  • Heidarieh M, Mirvaghefi AR, Akbari M, Farahmand H, Sheikhzadeh N, Shahbazfar AA, Behgar M (2012) Effect of dietary Ergosan on growth performance, digestive enzymes, intestinal histology, hematological parameters and body composition of rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 38:1169–1174

    Article  CAS  Google Scholar 

  • Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597

    Article  CAS  Google Scholar 

  • Julshamn K, Dahl L, Eckhoff K (2001) Determination of iodine in seafood by inductively coupled plasma/mass spectrometry. J AOAC Int 84:1976–1983

    CAS  PubMed  Google Scholar 

  • Mæhre HK, Malde MK, Eilertsen KE, Elvevoll EO (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

    Article  Google Scholar 

  • Marinho G, Nunes C, Sousa-Pinto I, Pereira R, Rema P, Valente LMP (2013) The IMTA-cultivated Chlorophyta Ulva spp. as a sustainable ingredient in Nile tilapia (Oreochromis niloticus) diets. J Appl Phycol 25:1359–1367 3

    Article  CAS  Google Scholar 

  • McNamara R, Jandacek R, Rider T, Tso P, Straus A, Lipton J (2010) Omega-3 fatty acid deficiency increases constitutive pro-inflammatory cytokine production in rats: relationship with central serotonin turnover. Prostaglandins Leukot Essent Fatty Acids 83:185–191

    Article  CAS  Google Scholar 

  • Morais S, Aragão C, Cabrita E, Conceição LEC, Constenla M, Costas B, Dias J, Duncan N, Engrola S, Estevez A, Gisbert E, Mañanós E, Valente LMP, Yúfera M, Dinis MT (2016) New developments and biological insights into the farming of Solea senegalensis reinforcing its aquaculture potential. Rev Aquacult 8:227–263

    Article  Google Scholar 

  • Mustafa MG, Wakamatsu S, Takeda TA, 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 

  • Nakagawa H, Nematipour GR, Yamamoto M (1993) Optimum level of Ulva meal diet supplement to minimize weight loss during wintering in black sea bream Acanthopagrus schlegeli (Bleeker). Asian Fish Sci 6:139–148

    Google Scholar 

  • Niu J, Chen X, Lu X, Jiang S-G, Lin H-Z, Liu Y-J, Huang Z, Wang J, Wang Y, Tian L-X (2015) Effects of different levels of dietary wakame (Undaria pinnatifida) on growth, immunity and intestinal structure of juvenile Penaeus monodon. Aquaculture 435:78–85

    Article  Google Scholar 

  • Norambuena F, Hermon K, Skrzypczyk V, Emery JA, Sharon Y, Beard A, Turchini GM (2015) Algae in fish feed: performances and fatty acid metabolism in juvenile Atlantic Salmon. PLoS One 10:e0124042

    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 

  • Peteiro C, Freire Ó (2011) Effect of water motion on the cultivation of the commercial seaweed Undaria pinnatifida in a coastal bay of Galicia, Northwest Spain. Aquaculture 314:269–276

    Article  Google Scholar 

  • Peteiro C, Sánchez N, Martínez B (2016) Mariculture of the Asian kelp Undaria pinnatifida and the native kelp Saccharina latissima along the Atlantic coast of Southern Europe: an overview. Algal Res 15:9–23

    Article  Google Scholar 

  • Pirarat N, Pinpimai K, Endo M, Katagiri T, Ponpornpisit A, Chansue N, Maita M (2011) Modulation of intestinal morphology and immunity in Nile tilapia (Oreochromis niloticus) by Lactobacillus rhamnosus GG. Res Vet Sci 91:e92–e97

    Article  CAS  Google Scholar 

  • Ribeiro AR, Gonçalves A, Bandarra N, Nunes ML, Dinis MT, Dias J, Rema P (2017) Natural fortification of trout with dietary macroalgae and selenised-yeast increases the nutritional contribution in iodine and selenium. Food Res Int 99

  • Ribeiro AR, Gonçalves A, Colen R, Nunes ML, Dinis MT, Dias J (2015) Dietary macroalgae is a natural and effective tool to fortify gilthead seabream fillets with iodine: effects on growth, sensory quality and nutritional value. Aquaculture 437:51–59

    Article  Google Scholar 

  • Rodiles A, Herrera M, Hachero-Cruzado I, Ruiz-Jarabo I, Mancera JM, Cordero ML, Lall SP, Alarcón FJ (2014) Tissue composition, blood biochemistry and histology of digestive organs in Senegalese sole (Solea senegalensis) juveniles fed diets containing different plant protein ingredients. Aquac Nutr 21:767–779

    Article  Google Scholar 

  • Rodríguez HP, Rojas SM (2014) Effect of diets enriched with vitamin E and organic selenium on the productive performance and meat quality of rainbow trout (Oncorhynchus mykiss). Rev Investig Vet Perú 25

  • Sánchez-Machado DI, López-Cervantes J, López-Hernández J, Paseiro-Losada P (2004) Fatty acids, total lipid, protein and ash contents of processed edible seaweeds. Food Chem 85:439–444

    Article  Google Scholar 

  • Schmid S, Ranz D, He ML, Burkard S, Lukowicz MY, reiter R, Arnold R, Le Deit H, David M, Rambeck WA (2003) Marine algae as natural source of iodine in the feeding of freshwater fish—a new possibility to improve iodine supply of man. Revue Méd Vét 154:645–648

    CAS  Google Scholar 

  • Silva DM, Valente LMP, Sousa-Pinto I, Pereira R, Pires MA, Seixas F, Rema P (2015) Evaluation of IMTA-produced seaweeds (Gracilaria, Porphyra, and Ulva) as dietary ingredients in Nile tilapia, Oreochromis niloticus L., juveniles. Effects on growth performance and gut histology J Appl Phycol 27:1s671–1680

  • Valente LM, 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 

  • Valente LMP, Linares F, Villanueva JLR, Silva JMG, Espe M, Escórcio C, Pires MA, Saavedra MJ, Borges P, Medale F, Alvárez-Blázquez B, Peleteiro JB (2011) Dietary protein source or energy levels have no major impact on growth performance, nutrient utilisation or flesh fatty acids composition of market-sized Senegalese sole. Aquaculture 318:128–137

    Article  CAS  Google Scholar 

  • Valente LMP, Rema P, Ferraro V, Pintado M, Sousa-Pinto I, Cunha LM, Oliveira MB, Araújo M (2015) Iodine enrichment of rainbow trout flesh by dietary supplementation with the red seaweed Gracilaria vermiculophylla. Aquaculture 446:132–139

    Article  CAS  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 71:39–45

    Article  Google Scholar 

  • Wassef EA, El-Sayed AFM, Kandeel KM, Sakr EM (2005) Evaluation of Pterocladia (Rhodophyta) and Ulva (Chlorophyta) meals as additives to gilthead seabream Sparus aurata diets. Egypt J Aquat Res 31:321–332

    Google Scholar 

  • Wassef EA, El-Sayed A-FM, Sakr EM (2013) Pterocladia (Rhodophyta) and Ulva (Chlorophyta) as feed supplements for European seabass, Dicentrarchus labrax L., fry. J Appl Phycol 25:1369–1376

    Article  CAS  Google Scholar 

  • Wassef EA, El Masry MH, 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 

  • WHO (2007) Assessment of iodine deficiency disorders and monitoring their elimination: a guide for programme managers, 3rd edn. World Health Organization, Geneva

  • Yi Y-H, Chang Y-J (1994) Physiological effects of seamustard supplement diet on the growth and body composition of young rockfish Sebastes schlegeli. Bull Korean Fish Soc 27:69–82

    Google Scholar 

  • Yildirim Ö, Ergün S, Yaman S, Türker A (2009) Effects of two seaweeds (Ulva lactuca and Enteromorpha linza) as a feed additive in diets on growth performance, feed utilization, and body composition of rainbow trout (Oncorhynchus mykiss). Kafkas Univ Vet Fak Derg 15:455–460

    Google Scholar 

  • Yone Y, Furuichi M, Urano K (1986a) Effects of dietary wakame Undaria penatifida and Ascophyllum nodosum supplements on growth, feed efficiency, and proximate composition of liver and muscle of red sea bream. Bull Jpn Soc Sci Fish 52:1465–1468

    Article  Google Scholar 

  • Yone Y, Furuichi M, Urano K (1986b) 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. Bull Jpn Soc Sci Fish 52:1817–1819

    Article  Google Scholar 

  • Zhu D, Wen X, Xuan X, Li S, Li Y (2016) The green alga Ulva lactuca as a potential ingredient in diets for juvenile white spotted snapper Lutjanus stellatus Akazaki. J Appl Phycol 28:703–711

    Article  CAS  Google Scholar 

  • Zimmermann MB, Jooste PL, Pandav CS (2008) Iodine-deficiency disorders. Lancet 372:1251–1262

    Article  CAS  Google Scholar 

Download references

Funding

This study was partially supported by MARINALGAE4aqua “Improving bio-utilisation of marine algae as sustainable feed ingredients to increase efficiency and quality of aquaculture production” ERA-NET COFASP/004/2015 and by the Structured R&D&I Project INNOVMAR—Innovation and sustainability in the management and exploitation of marine resources (ref. NORTE-01-0145-FEDER-000035) within the research line “INSEAFOOD—Innovation and valorization of seafood products: meeting local challenges and opportunities”, founded by the Northern Regional Operational Programme (NORTE2020) through the European Regional Development Fund (ERDF).

Author information

Authors and Affiliations

  1. CIIMAR, Centro Interdisciplinar de Investigação Marinha e Ambiental, Universidade do Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Nórton de Matos, S/N, 4450-208, Matosinhos, Portugal

    S. Moutinho, Vera Sousa & L. M. P. Valente

  2. CIMA, Centro de Investigacións Mariñas, Pedras de Corón s/n. Apdo. 13, Vilanova de Arousa, 36620, Pontevedra, Spain

    F. Linares

  3. IGAFA, Instituto Galego de formación en Acuicultura, Niño do Corvo, s/n. Illa de Arousa, 36626, Pontevedra, Spain

    J. L. Rodríguez

  4. ICBAS, Instituto de Ciências Biomédicas de Abel Salazar, Universidade do Porto, Rua de Jorge Viterbo Ferreira, 228, 4050-313, Porto, Portugal

    Vera Sousa & L. M. P. Valente

Authors
  1. S. Moutinho
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Linares
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. L. Rodríguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vera Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. L. M. P. Valente
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. M. P. Valente.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moutinho, S., Linares, F., Rodríguez, J.L. et al. Inclusion of 10% seaweed meal in diets for juvenile and on-growing life stages of Senegalese sole (Solea senegalensis). J Appl Phycol 30, 3589–3601 (2018). https://doi.org/10.1007/s10811-018-1482-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-018-1482-6

Keywords

Search

Navigation