Skip to main content
Log in

Effects of partial replacement of fishmeal protein with green seaweed (Cladophora spp.) protein in practical diets for the black tiger shrimp (Penaeus monodon) postlarvae

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

Abstract

This study assessed the effects of the green seaweed Cladophora spp. as a protein source to substitute fishmeal protein in practical diets for postlarval tiger shrimp (Penaeus monodon). A control diet without containing seaweed meal was compared with five experimental diets in which fishmeal protein was replaced by increasing the levels of green seaweed protein (10, 20, 30, 40 and 50%) in the diets. All diets were formulated to be equivalent in crude protein (40%) and lipid (7%). Each dietary treatment was replicated in triplicate. After 45 days of the feeding trial, survival of the shrimp was not significantly influenced by the feeding treatments (p > 0.05). Growth rates of the shrimp fed with 10, 20, or 30% replacement levels of green seaweed protein in the diets were superior or similar to those fed with the control diet whereas shrimp fed with the diet containing 40 and 50% substitution levels showed significant reduction in growth (p < 0.05). The feed conversion ratio and protein efficiency ratio exhibited the similar trend as observed for growth performance. Moreover, shrimp fed with the control diet presented the lowest stress tolerance to formalin shock while the best performance was detected in the animals that received the 10 and 20% replacement diet. These results suggested that green seaweed Cladophora could replace up to 30% of fishmeal protein in the tiger shrimp postlarvae diet, and the optimal performance, including growth rate, feed efficiency, and stress resistance, appeared in shrimp fed with the diet of 10 to 20% substitution.

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.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Anh NTN, Toan NT, Hai TN (2013) Potential use of dried gut weed (Enterormorpha sp.) and blanket weed (Cladophoraceae) as a feed for the giant gourami (Osphronemus goramy) (abstract in English). Can Tho Uni J Sci 35:1040–1110

    Google Scholar 

  • Anh NTN, Nhung DTK, Hai TN (2014) Replacement of soybean meal protein with gut weed (Enteromorpha sp.) and blanket weed (Cladophoracae) protein in practical diets for the white leg shrimp (Litopenaeus vannamei) postlarvae (abstract in English). Can Tho Uni J Sci 2:1580–1165

    Google Scholar 

  • Anh NTN, Hong DT, Hai TN (2016) Investigating abundance and impacts of green seaweed (Cladophoraceae) in the improved extensive shrimp farms in Mekong delta. International Fisheries Symposium – IFS 2016 Promoting Healthier Aquaculture and Fisheries for Food Safety and Security. Phu Quoc Island of Vietnam, 31st October to 2nd November 2016, p 248

  • AOAC (2000) Official methods of analysis. Association of Official Analytical Chemists, Arlington 159 pp

    Google Scholar 

  • Arnold SJ, Sellars MJ, Crocos PJ, Coman GJ (2006) Intensive production of juvenile tiger shrimp Penaeus monodon: an evaluation of stocking density and artificial substrates. Aquaculture 261:890–896

    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 

  • Beiping T, Kangsen M, Shixuan Z, Qicun Z, Lihe L, Yu Y (2005) Replacement of fish meal by meat and bone meal in practical diets for the white shrimp Litopenaeus vannamei (Boone). Aquac Res 36:439–444

    Article  Google Scholar 

  • Briggs MRP, Funge-Smith SL (1996) The potential of Gracilaria spp. meal for supplementation of diets for juvenile Penaeus monodon Fabricius. Aquac Res 27:345–354

    Article  Google Scholar 

  • Brinkera A, Reiter R (2011) Fish meal replacement by plant protein substitution and guar gum addition in trout feed, part I: effects on feed utilization and fish quality. Aquaculture 10:350–360

    Article  CAS  Google Scholar 

  • Burtin P (2003) Nutritional value of seaweeds. Elect J Env Agricult Food Chem 2:1–6

    Google Scholar 

  • Cárdenas JV, Gálvez AO, Brito LO, Galarza EV, Pitta DC, Rubin VV (2015) Assessment of different levels of green and brown seaweed meal in experimental diets for whiteleg shrimp (Litopenaeus vannamei, Boone) in recirculating aquaculture system. Aquac Int 23:1491–1504

    Article  CAS  Google Scholar 

  • Chien YH, Pan CH, Hunter B (2003) The resistance to physical stresses by Penaeus monodon juveniles fed diets supplemented with astaxanthin. Aquaculture 216:177–191

    Article  CAS  Google Scholar 

  • Cruz-Suárez LE, Tapia-Salazar M, Nieto-Lopez MG, Ricque-Marie D (2008) A review of the effect of macroalgae in shrimp feed and in co-culture. IX Simposio Internacional de Nutricion Acuicola, 24-27 Noviembre, Universidad Autonoma de Nuevo Leon, Monterrey, Nuevo Leon, Mexico:304-333

  • Cruz-Suárez LE, Tapia-Salazar M, Nieto-Lopez MG, Guajardo-Barbosa C, Ricque-Marie D (2009) Comparison of Ulva clathrata and the kelps Macrocystis pyrifera and Ascophyllum nodosum as ingredients in shrimp feeds. Aquac Nutr 15:421–430

    Article  CAS  Google Scholar 

  • da Silva RL, Barbosa JM (2009) Seaweed meal as a protein source for the white shrimp Litopenaeus vannamei. J Appl Phycol 21:193–197

    Article  Google Scholar 

  • Davis DA, Sookying D (2009) Strategies for reducing and/or replacing fish meal in production diets for the Pacific white shrimp, Litopenaeus vannamei. In: Browdy CL, Jory DE (eds) The rising tide, proceedings of the special session on shrimp farming. World Aquaculture Society, Baton Rouge, pp 91–96

    Google Scholar 

  • Dhargalkar VK, Neelam P (2005) Seaweed: promising plant of the millennium. Sci Cult 71:60–66

    Google Scholar 

  • Elizondo-Reyna E, Medina-González R, Nieto-López MG, Ortiz-López R, Elizondo-González R, Powell MS, Ricque-Marie D, Cruz-Suárez LE (2016) Consumption of Ulva clathrata as a dietary supplement stimulates immune and lipid metabolism genes in Pacific white shrimp Litopenaeus vannamei. J Appl Phycol 28:3667–3677

    Article  CAS  Google Scholar 

  • Felix N, Brindo RA (2014) Substituting fishmeal with fermented seaweed, Kappaphycus alvarezii in diets of juvenile freshwater prawn Macrobrachium rosenbergii. Int J Fish Aquat Stud 1:261–265

    Google Scholar 

  • Ghosh R, Mitra A (2015) Suitability of green macroalgae Enteromorpha intestinalis as a feed form Macrobrachium rosenbergii. J Fish Livest Prod 3:138

    Google Scholar 

  • Glencross BD, Booth M, Allan GL (2007) A feed is only as good as its ingredients—a review of ingredient evaluation for aquaculture feeds. Aquac Nutr 13:17–34

    Article  CAS  Google Scholar 

  • Hafezieh M, Ajdari D, Ajdehakosh PA, Hosseini SH (2014) Using Oman Sea Sargassum illicifolium meal for feeding white leg shrimp Litopenaeus vannamei. Iran J Fish Sci 13:73–80

    Google Scholar 

  • Hai TN, Minh TH, Phu TQ, Phuong NT (2016) Shrimp industry in Vietnam. In: Liao IC, Chao NH, Leaño EM (ed) Progress of shrimp and prawn aquaculture in the world. National Taiwan University, the Fisheries Society of Taiwan, Asian Fisheries Society, and World Aquaculture Society, pp 181–204

  • ITB-Vietnam (2011) Study on distribution and culture of seaweeds and aquatic plants in the Mekong delta, Vietnam. International co-operation plan. Algen Sustainable & Center Novem, Netherlands

    Google Scholar 

  • Khuantrairong T, Traichaiyaporn S (2011) The nutritional value of edible freshwater alga Cladophora sp. (Chlorophyta) grown under different phosphorus concentrations. Int J Agric Biol 13:1560–8530

    Google Scholar 

  • Khuantrairong T, Traichaiyaporn S (2012) Enhancement of carotenoid and chlorophyll content of an edible freshwater alga (Kai: Cladophora sp.) by supplementary inorganic phosphate and investigation of its biomass production. Maejo Int J Sci Technol 6:1–11

    CAS  Google Scholar 

  • Kumar V, Kaladharan P (2007) Amino acids in the seaweeds as an alternate source of protein for animal feed. J Mar Biol Assoc India 49:35–40

    Google Scholar 

  • Lan NTP (2013) Social and ecological challenges of market-oriented shrimp farming in Vietnam. Spring 2:675

    Article  Google Scholar 

  • Meyers SP (1994) Developments in world aquaculture, feed formulations and role of carotenoids. Pure Appl Chem 66:1069–1076

    Article  CAS  Google Scholar 

  • Millamena OM, Bautista-Teruel MN, Kanazawa A (1996) Methionine requirement of juvenile tiger shrimp Penaeus monodon Fabricius. Aquaculture 143:403–410

    Article  CAS  Google Scholar 

  • Millamena OM, Bautista-Teruel MN, Reyes OS, Kanazawa A (1998) Requirements of juvenile marine shrimp, Penaeus monodon (Fabricius) for lysine and arginine. Aquaculture 164:95–104

    Article  CAS  Google Scholar 

  • Molina–Poveda C, Morales ME (2004) Use of a mixture of barley–based fermented grains and wheat gluten as an alternative protein source in practical diets for Litopenaeus vannamei. Aquac Res 35:1158–1165

    Article  CAS  Google Scholar 

  • Olsen RL, Hasan MR (2012) A limited supply of fishmeal: impact on future increases in global aquaculture production. Trends Food Sci Technol 27:120–128

    Article  CAS  Google Scholar 

  • Pallaoro MF, do Nascimento Vieira F, Hayashi L (2016) Ulva lactuca (Chlorophyta Ulvales) as co-feed for Pacific white shrimp. J Appl Phycol 28:3659–3665

    Article  CAS  Google Scholar 

  • Peixoto MJ, Salas-Leitóna E, Pereiraa LF, Queiroza A, Magalhãesa F, Pereirad R, Abreu H, Reis P, Goncalves JFM, Ozórioa ROA (2016) Role of dietary seaweed supplementation on growth performance, digestive capacity and immune and stress responsiveness in European seabass (Dicentrarchus labrax). Aquac Rep 3:189–197

    Article  Google Scholar 

  • Portley N (2016) Report on the shrimp sector: Asian shrimp trade and sustainability. Sustainable Fisheries Partnership. https://www.sustainablefish.org/. Accessed 14 Jun 2017

  • Potty HV (1996) Physio-chemical aspects, physiological functions, nutritional importance and technological significance of dietary fibres a critical appraisal. J Food Sci Technol 33:1–18

    CAS  Google Scholar 

  • Pushparajan N, Soundarapandian P (2010) Recent farming of marine black tiger shrimp, Penaeus monodon (Fabricius) in South India. Afr J Basic Appl Sci 2:33–36

    Google Scholar 

  • Qiu X, Neori A, Kim JK, Yarish C, Shpigel M, Guttman L, Ben Ezra D, Odintsov V, Davis DA (2017) Green seaweed Ulva sp. as an alternative ingredient in plant-based practical diets for Pacific white shrimp, Litopenaeus vannamei. J Appl Phycol. https://doi.org/10.1007/s10811-017-1288-y

  • Rivera G, Yoong F, Riofrio G, Reinoso B, Hurtado F, Massuh P (2002). Inclusión de harina de kelp (Macrocystis pyrifera) en alimentos balanceados para el camarón. Congreso Iberiamericano Virtual de Acuícultura. CIVA. http://www.civa2002.org, searched on 26 June 2013

  • Rodríguez-González H, Orduña-Rojas, Villalobos-Medina JP, García-Ulloa M, Polanco-Torres A, López-Álvarez ES, Montoya-Mejía M, Hernández-Llamas A (2014) Partial inclusion of Ulva lactuca and Gracilaria parvispora meal in balanced diets for white leg shrimp (Litopenaeus vannamei). J Appl Phycol 26:2453–2459

    Article  CAS  Google Scholar 

  • Samocha TM, Guajardob H, Lawrence AL, Castillec FL, Speedd M, McKee DA, Pagee KI (1998) A simple stress test for Penaeus vannamei postlarvae. Aquaculture 165:233–242

    Article  Google Scholar 

  • Santizo R, Serrano AE Jr, Corre VL (2014) Proximate composition and dry matter digestibility of Ulva lactuca in the black tiger shrimp Penaeus monodon. ABAH Bioflux 6:75–83

    Google Scholar 

  • Serrano AE Jr, Santizo R (2014) Dietary substitution of protein concentrate of Ulva lactuca for soybean meal in the black tiger shrimp Penaeus monodon fry. ABAH Bioflux 6:140–147

    Google Scholar 

  • Serrano AE Jr, Tumbokomn BLM (2015) Optimum dietary inclusion of Ulva intestinalis to the diet of the black tiger shrimp Penaeus monodon postlarvae. AACL Bioflux 7:169–176

    CAS  Google Scholar 

  • Serrano AE Jr, Santizo RB, Tumbokon BLM (2015) Potential use of the sea lettuce Ulva lactuca replacing soybean meal in the diet of the black tiger shrimp Penaeus monodon juvenile. AACL Bioflux 8:245–252

    Google Scholar 

  • Smith DM, Allan GL, Williams KC and Barlow C (2000) Fishmeal replacement research for shrimp feed in Australia. In: Cruz-Suárez LE, Ricque-Marie D, Tapia-Salazar M, Olvera-Novoa MA, Civera-Cerecedo R, (eds) Avances en Nutrición Acuícola V. Memorias del V Simposium Internacional de Nutrición Acuícola. 19-22 Noviembre, 2000. Mérida, Yucatán, México

  • Soltani S, Saadatmand S, Khavarinejad R, Nejadsattari T (2011) Antioxidant and antibacterial activities of Cladophora glomerata (L.) Kütz. in Caspian Sea coast, Iran. Afr J Biotechnol 10:7684–7689

    CAS  Google Scholar 

  • Stabili L, Acquaviva MI, Biandolino F, Cavallo RA, De Pascali SA, Fanizzi FP, Narracci M, Cecere E, Petrocelli A (2014) Biotechnological potential of the seaweed Cladophora rupestris (Chlorophyta, Cladophorales) lipidic extract. Nat Biotechnol 31:436–444

    CAS  Google Scholar 

  • Sudaryono A, Haditomo AH, Isnansetyo A (2015) Evaluation of dietary supplementation of aqueous extract of brown algae Sargassum cristaefolium on growth performance and feed utilization of juvenile white shrimp Litopenaeus vannamei. AACL Bioflux 8:142–149

    Google Scholar 

  • Teshima S, Ishikawa M, Koshio S (2000) Nutritional assessment and feed intake of microparticulate diets in crustaceans and fish. Aquac Res 31:691–702

    Article  Google Scholar 

  • Thanh T, Nghia TT, Phuong NT (2002) Advanced technologies for shrimp larviculture of Penaeus monodon in the bio-filter system (abstract in English). Can Tho Uni J Sci 2:185–190

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Yahyavi M, Takami GHA, Vosoughi GH (2007) The study of salinity and formalin stress tests in postlarval feeding of Indian white shrimp by enriched rotifers with unsaturated fatty acids (DHA, EPA) and vitamin C. JWSS 10:519–531

    CAS  Google Scholar 

  • Zbakh H, Chiheb I, Motilva V, Riadi H (2014) Antibacterial, cytotoxic and antioxidant potentials of Cladophora prolifera (Roth) Kutzing collected from the Mediterranean coast of Morocco. Am J Phytomed Clin Therapeut 2:1187–1199

    Google Scholar 

  • Zorriehzahra MJ, Banaederakhshan R (2015) Early mortality syndrome (EMS) as new emerging threat in shrimp industry. Adv Anim Vet Sci 3:64–72

    Article  Google Scholar 

Download references

Acknowledgments

The authors sincerely thank Dr. Nguyen Xuan Hoa, Nha Trang Institute of Oceanography and Ms. Huynh Ly Huong for their help in identifying the genus of green seaweed and Le Thanh Y for his help during the feeding trial.

Funding

This study was funded by the Vietnamese Ministry of Education and Training for the scientific research programs.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nguyen Thi Ngoc Anh.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Anh, N.T.N., Hai, T.N. & Hien, T.T.T. Effects of partial replacement of fishmeal protein with green seaweed (Cladophora spp.) protein in practical diets for the black tiger shrimp (Penaeus monodon) postlarvae. J Appl Phycol 30, 2649–2658 (2018). https://doi.org/10.1007/s10811-018-1457-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-018-1457-7

Keywords

Navigation