Digestibility and gastrointestinal transit of Ulva fasciata seaweed meal in tilapia (Oreochromis niloticus) juveniles: basis for the inclusion of a sustainable ingredient in aquafeeds
DOI:
https://doi.org/10.33448/rsd-v9i10.8497Keywords:
Macroalgae; Complementary ingredient; Fish feed; Non-starch polysaccharides; Ulvan; Integrated multi-trophic aquaculture.Abstract
The seaweed Ulva fasciata has many features favorable to integrated multi-trophic aquaculture (IMTA). It is efficient at biofiltering, shows high biomass production, and is rich in many nutrients useful in aquatic animal diets. We evaluated the digestibility of the seaweed meal of U. fasciata produced in IMTA and its effects on gastrointestinal transit time in tilapia (Oreochromis niloticus) juveniles. Juveniles (6.30 ± 1.80 g initial weight, and 5.5 ± 0.61 cm initial length) were cultivated in six tanks (50 individuals per tank) in a closed recirculating aquaculture system. The digestibility of Ulva meal was 57.92 ± 5.21% for dry material, 78.59 ± 1.91% for protein, and 69.87 ± 3.72% for energy. The inclusion of 10% seaweed meal did not alter the gastrointestinal transit time in tilapia juveniles as compared to controls. The earliest colored feces were observed four hours after first feeding in both treatments (feed diets with [10%] and without seaweed); all fecal material was colored after ten hours. The digestibility of seaweed meal was satisfactory for dry material, protein, and gross energy, and the inclusion of 10% of that meal did not change gastrointestinal transit time - indicating that the inclusion of 10% seaweed meal in tilapia diet is safe and without any nutritional use losses.
References
Amirkolaie, A. K., Verreth, J. A., Schrama, J. W. (2006). Effect of gelatinization degree and inclusion level of dietary starch on the characteristics of digesta and faeces in Nile tilapia (Oreochromis niloticus (L.)). Aquaculture, 260, 194-205.
Azaza, M. S., Mensi, F., Ksouri, J., Dhraief, M. N., Brini, B., Abdelmouleh, A., Kraiem, M. M. (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. Journal of Applied Ichthyology, 24, 202-207.
Ben-Ari, T., Neori, A., Ben-Ezra, D., Shauli, L., Odintsov, V., Shpigel, M. (2014) Management of Ulva lactuca as a biofilter of mariculture effluents in IMTA system. Aquaculture, 434, 493–498.
Calheiros, A. C., Reis, R. P., Castelar, B., Cavalcanti, D. N., Teixeira, V. L. (2019). Ulva spp. as a natural source of phenylalanine and tryptophan to be used as anxiolytics in fish farming. Aquaculture, 509, 171-177.
Carneiro, D. J., Rantin, R. T., Dias, T. C. R., Malheiros, E. B. (1994). Interaction between temperature and dietary levels of protein and energy in pacu (Piaractus mesopotamicus). II. Effects on digestibility of protein and transit time through the gastrointestinal tract. Aquaculture, 124.
Castelar, B., Reis, R. P., & dos Santos Calheiros, A. C. (2014). Ulva lactuca and U. flexuosa (Chlorophyta, Ulvophyceae) cultivation in Brazilian tropical waters: recruitment, growth, and ulvan yield. Journal of applied phycology, 26(5), 1989-1999.
Castelar, B., Pontes, M. D., Costa, W. M., Fontes, L. C., Dias, G. E., Landuci, F. E. & Reis, R. P. (2015). Biofiltering efficiency and productive performance of macroalgae with potential for integrated multi-trophic aquaculture (IMTA). Boletim do Instituto de Pesca, 41, 763 – 770.
CBAA (2009). Compêndio brasileiro de alimentação animal. Sindirações (Ed). São Paulo, 390p.
Cheng, Z. J., Hardy, R. W. (2003). Effects of extrusion processing of feed ingredients on apparent digestibility coefficients of nutrients for rainbow trout (Oncorhynchus mykiss). Aquaculture nutrition, 9, 77-83.
Cruz-Suárez, L. E, León, A., Peña-Rodríguez, A., Rodríguez-Peña, G., Moll, B., Ricque-Marie, D. (2010). Shrimp/Ulva co-culture: a sustainable alternative to diminish the need for artificial feed and improve shrimp quality. Aquaculture 301, 64–68.
Diamahesa, W. A., Masumoto, T., Jusadi, D., Setiawati, M. (2017). Growth and protein content of Ulva Prolifera maintained at different flow rates in integrated aquaculture system. Jurnal Ilmu dan Teknologi Kelautan Tropis, 9(2), 429-441.
El-Tawil, N. E. (2010). Effects of green seaweeds (Ulva sp.) as feed supplements in red Tilapia (Oreochromis sp.) diet on growth performance, feed utilization and body composition. Journal of the Arabian Aquaculture Society, 5,179-193.
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. Aquaculture International, 17, 355-361.
Felix, N., Brindo, R. A. (2014). Evaluation of raw and fermented seaweed, Ulva lactuca as feed ingredient in giant freshwater prawn Macrobrachium rosenbergii. International Journal of Fisheries and Aquatic Studies, 1, 199-204.
Fleurence, J. (1999). Seaweed proteins: biochemical, nutritional aspects and potential uses, Trends in Food Science & Technology, 10, 25-28.
Francis, G., Makkar, H. P., Becker, K. (2001). Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture,199, 197-227.
Furuya, W. M., Pezzato, L. E., Miranda, E. C., Furuya, V. R. B., Barros, M. M. (2001). Coeficientes de digestibilidade aparente da energia e nutrientes de alguns ingredientes pela tilápia do Nilo, Oreochromis niloticus (L.)(linhagem tailandesa). Acta Scientiarum, 23, 465-469.
Gentelini, A. L., Boscolo, W. R., Feiden, A., Meurer, F., Hayashi, C. (2005). Graus de moagem dos ingredientes em rações peletizadas para alevinos de piavuçu (Leporinus macrocephalus). Acta Scientiarum Animal Sciences, 27, 93-97.
Güroy, B. K., Cirik, Ş., Güroy, D., Sanver, F., Tekinay, A. A. (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. Turkish Journal of Veterinary and Animal Sciences, 31, 91-97.
Haidar, M. N., Petie, M., Heinsbroek, L. T., Verreth, J. A., Schrama, J. W. (2016). The effect of type of carbohydrate (starch vs. nonstarch polysaccharides) on nutrients digestibility, energy retention and maintenance requirements in Nile tilapia. Aquaculture, 463, 241-247.
Hayashi, C., Boscolo, W. R., Soares, C. M., Boscolo, V. R., Galdioli, E. M. (1999). Uso de diferentes graus de moagem dos ingredientes em dietas para a tilápia-do-Nilo (Oreochromis niloticus L.) na fase de crescimento. Acta Scientiarum. Animal Sciences, 21, 733-737.
Jobling, M., Gwyther, D., Grove, D. J. (1977). Some effects of temperature, meal size and body weight on gastric evacuation time in the dab Limanda limanda (L). Journal of Fish Biology, 10, 291-298.
Lahaye, M., Robic, A. (2007). Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules, 8, 1765-1774
Lanna, E. A. T., Pezzato, L. E., Cecon, P. R., Furuya, W. M., Bomfim, M. A. D. (2004). Digestibilidade aparente e trânsito gastrintestinal em tilápia do Nilo (Oreochromis niloticus), em função da fibra bruta da dieta. Revista Brasileira de Zootecnia, 33, 2186-2192.
Leenhouwers, J. I., Adjei Boateng, D., Verreth, J. A. J., Schrama, J. W. (2006). Digesta viscosity, nutrient digestibility and organ weights in African catfish (Clarias gariepinus) fed diets supplemented with different levels of a soluble non starch polysaccharide. Aquaculture Nutrition, 12, 111-116.
Marinho, G., Nunes, C., Sousa-Pinto, I., Pereira, R., Rema, P., Valente, L. M. 2013. The IMTA-cultivated Chlorophyta Ulva spp. as a sustainable ingredient in Nile tilapia (Oreochromis niloticus) diets. Journal of applied phycology, 25, 1359-1367.
Meurer, F., Hayashi, C., Boscolo, W. R., Soares, C. M. (2002). Lipídeos na alimentação de alevinos revertidos de tilápia do Nilo (Oreochromis niloticus L.). Revista Brasileira de Zootecnia, 31, 566-573.
Meurer, F., Hayashi, C., Boscolo, W. R. (2003). Fibra bruta para alevinos de tilápia do Nilo (Oreochromis niloticus, L). Revista Brasileira de Zootecnia, 32, 256-261.
Montagne, L., Pluske, J. R., Hampson, D. J. (2003). A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals. Animal feed science and technology, 108, 95-117.
Msuya, F. E., Neori, A. (2008). Effect of water aeration and nutrient load level on biomass yield, N uptake and protein content of the seaweed Ulva lactuca cultured in seawater tanks. Journal of Applied Phycology, 20, 1021-1031.
Nielsen, M. M., Bruhn, A., Rasmussen, M. B., Olesen, B., Larsen, M. M., Møller, H. B. (2012) Cultivation of Ulva lactuca with manure for simultaneous bioremediation and biomass production. Journal of Applied Phycology, 24, 449–458.
Oca, J., Cremades, J., Jiménez, P., Pintado, J., Masaló, I. (2019). Culture of the seaweed Ulva ohnoi integrated in a Solea senegalensis recirculating system: influence of light and biomass stocking density on macroalgae productivity. Journal of Applied Phycology, 3, 2461-2467.
Øverland, M., Mydland, L. T., & Skrede, A. (2019). Marine macroalgae as sources of protein and bioactive compounds in feed for monogastric animals. Journal of the Science of Food and Agriculture, 99(1), 13-24.
Pereira, R., Valente, L. M., Sousa-Pinto, I., Rema, P. (2012). Apparent nutrient digestibility of seaweeds by rainbow trout (Oncorhynchus mykiss) and Nile tilapia (Oreochromis niloticus). Algal Research, 1, 77-82.
Pezzato, L. E., Miranda, E. C. D., Barros, M. M., Pinto, L. G. Q., Furuya, W. M., Pezzato, A. C. (2002). Digestibilidade aparente de ingredientes pela tilápia do Nilo (Oreochromis niloticus). Revista Brasileira de Zootecnia, 31,1595-1604.
Quezada-Rodríguez, P. R., Fajer-Ávila, E. J. (2017). The dietary effect of ulvan from Ulva clathrata on hematological-immunological parameters and growth of tilapia (Oreochromis niloticus). Journal of Applied Phycology, 29, 423-431.
Rodrigues, L. A., Fabregat, T. E. H. P., Fernandes, J. B. K., Nascimento, T. M. T, Sakomura, N. K. (2010). Digestibilidade e tempo de trânsito gastrintestinal de dietas contendo níveis crescentes de fibra bruta para pacu. Acta Scientiarum. Animal Sciences, 32, 169-173.
Shpigel, M., Guttman, L., Ben-Ezra, D., Yu, J., Chen, S. (2019). Is Ulva sp. able to be an efficient biofilter for mariculture effluents? Journal of Applied Phycology, 31, 2449–2459.
Storebakken, T. (1985). Binders in fish feeds: I. Effect of alginate and guar gum on growth, digestibility, feed intake and passage through the gastrointestinal tract of rainbow trout. Aquaculture, 47, 11-26.
Sinha, A. K., Kumar, V., Makkar, H. P., De Boeck, G., Becker, K. (2011). Non-starch polysaccharides and their role in fish nutrition–A review. Food Chemistry, 127, 1409-1426.
Sugiura, S. H., Dong, F. M., Rathbone, C. K., Hardy, R. W. (1998). Apparent protein digestibility and mineral availabilities in various feed ingredients for salmonid feeds. Aquaculture, 159, 177-202.
Troell, M., Naylor, R. L., Metian, M., Beveridge, M., Tyedmers, P. H., Folke, C., Gren, Å. (2014). Does aquaculture add resilience to the global food system?. Proceedings of the National Academy of Sciences, 111, 13257-13263.
Turchini, G. M., Trushenski, J. T., Glencross, B. D. (2019). Thoughts for the future of aquaculture nutrition: realigning perspectives to reflect contemporary issues related to judicious use of marine resources in aquafeeds. North American Journal of Aquaculture 81(1), 13-39.
Valente, L. M., Araújo, M., Batista, S., Peixoto, M.J., Sousa-Pinto, I., Brotas, V., Rema, P. (2015). Carotenoid deposition, flesh quality and immunological response of Nile tilapia fed increasing levels of IMTA-cultivated Ulva spp. Journal of Applied Phycology, 28, 1-11.
Zar, J. H. (1996). Biostatistical Analysis. Prentice Hall. Upper Sadle River, NJ
Zhang, X., Wu, H., Li, Z., Li, Y., Wang, S., Zhu, D., Li, S. (2017). Effects of dietary supplementation of Ulva pertusa and non-starch polysaccharide enzymes on gut microbiota of Siganus canaliculatus. Chinese Journal of Oceanology and Limnology, 36, 438–449
Zhu, D., Wen, X., Xuan, X., Li, S., Li, Y. (2015). The green alga Ulva lactuca as a potential ingredient in diets for juvenile white spotted snapper Lutjanus stellatus Akazaki. Journal of Applied Phycology, 28, 703–711.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2020 Marcelo Duarte Pontes; Daniel Abreu Vasconcelos Campelo; Rodrigo Takata; Lidia Miyako Yoshii Oshiro; Beatriz Castelar
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.
