Microalgae as an Alternative Mineral Source in Poultry Nutrition
Abstract
:Simple Summary
Abstract
1. Introduction
2. An overview of Microalgae
3. Mineral Composition of Microalgae
Analysis | Arthrospira sp. | Chlorella sp. | Isochrysis sp. | Porphyridium sp. | Schizochytrium sp. |
---|---|---|---|---|---|
Ash (%) | 6.10–34.8 (9.87 ± 6.00) | 5.5–27.3 (10.7 ± 5.4) | 12.0–32.2 (18.7 ± 6.14) | 16.5–35.9 (23.1 ± 7.62) | 3.81–10.0 (7.37 ± 2.35) |
Macrominerals (g/kg) | |||||
Ca | 0.23–10.3 (3.45 ± 3.78) | 0.36–53.3 (9.32 ± 16.8) | 5.83–11.5 (9.37 ± 3.08) | 6.40–20.7 (12.8 ± 5.17) | 3.53 |
K | 10.9–29.1 (18.1 ± 5.84) | 0.01–133 (23.6 ± 41.6) | 4.10–13.1 (10.4 ± 4.22) | 6.70–13.5 (11.2 ± 2.69) | 5.71 |
Mg | 0.77–4.00 (2.72 ± 1.20) | 0.41–16.4 (5.56 ± 5.69) | 3.38–10.0 (6.07 ± 3.03) | 4.74–13.7 (7.41 ± 3.61) | NA |
Na | 4.80–96.2 (25.8 ± 26.0) | 0.07–16.5 (5.67 ± 6.81) | 11.1–27.4 (18.4 ± 8.26) | 8.10–70.7 (29.5 ± 27.4) | 1.04 |
P | 1.50–14.8 (9.10 ± 4.25) | 5.11–27.1 (16.4 ± 7.37) | 6.25–27.6 (15.5 ± 11.0) | 3.17–14.6 (10.5 ± 6.39) | 4.88 |
S | NA | 0.12 | NA | 6.40–14.8 (11.9 ± 4.76) | 7.68 |
Microminerals (mg/kg) | |||||
Cu | 0.40–18.7 (4.32 ± 6.54) | 0.00–119 (24.3 ± 35.4) | 6.00–28.0 (14.5 ± 9.75) | 7.86–45.3 (17.0 ± 15.9) | 2.08 |
Fe | 106–1036 (512 ± 357) | 187–5400 (1289 ± 1702) | 15.2–2284 (880 ± 1007) | 377–11,101 (2682 ± 4708) | 13.5 |
Mn | 13.0–550 (87.1 ± 174) | 20.9–1270 (269 ± 406) | 36.0–834 (272 ± 379) | 22.0–259 (81.1 ± 100) | NA |
Zn | 0.40–30.1 (16.2 ± 11.4) | 9.07–530 (131 ± 173) | 20.0–940 (280 ± 443) | 41.0–392 (199 ± 176) | 37.4 |
4. Impact of Microalgae on Poultry Performance and Egg and Meat Quality
5. Sustainability and Environmental Impact
6. Economic Viability
7. Safety and Regulatory Aspects
8. Conclusion and Future Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Smith, J.A. Mineral Requirements in Poultry Nutrition: A Comprehensive Review. Poult. Sci. J. 2018, 97, 34–44. [Google Scholar]
- Johnson, K. The Role of Trace Elements in Poultry Nutrition. Anim. Feed Sci. Technol. 2020, 268, 110–119. [Google Scholar]
- Brown, A.; Smith, D. Environmental Impact of Mineral Supplementation in Poultry Production. J. Sustain. Agric. 2019, 43, 456–468. [Google Scholar]
- Liu, Y. The Role of Organic Minerals in Poultry Nutrition. J. Anim. Sci. Feed Technol. 2018, 112, 204–212. [Google Scholar]
- Smith, A.K.; Jones, M.E. Cost-Effectiveness of Organic Mineral Supplementation in Poultry Diets. Glob. Poult. Res. J. 2017, 5, 114–120. [Google Scholar]
- Davies, S.J. Bioavailability Issues in Poultry Feed Minerals. Poult. World 2019, 3, 33–37. [Google Scholar]
- Green, T.J. Microalgae as Sustainable Feed Ingredients in Poultry Nutrition. Environ. Sustain. Agric. 2018, 4, 58–67. [Google Scholar]
- Johnson, L.R. Microalgae in Animal Feed: Opportunities and Challenges. Feed. Nutr. Mag. 2020, 12, 22–28. [Google Scholar]
- Patel, A.; Kim, J.J. Microalgae in Poultry Feed: Opportunities and Challenges. J. Anim. Sci. Biotechnol. 2019, 10, 30. [Google Scholar]
- Lee, Y.-K. Microalgal mass culture systems and methods: Their limitation and potential. J. Appl. Phycol. 2001, 13, 307–315. [Google Scholar] [CrossRef]
- Becker, E.W. Micro-algae as a source of protein. Biotechnol. Adv. 2007, 25, 207–210. [Google Scholar] [CrossRef] [PubMed]
- Caporgno, M.P.; Mathys, A. Trends in microalgae incorporation into innovative food products with potential health benefits. Front. Nutr. 2018, 5, 58. [Google Scholar] [CrossRef] [PubMed]
- Fields, F.J. Biofortification of Microalgae for Nutritional Enhancement: A Review. Algal Res. 2020, 45, 101748. [Google Scholar]
- Borowitzka, M.A. High-value products from microalgae—Their development and commercialisation. J. Appl. Phycol. 2013, 25, 743–756. [Google Scholar] [CrossRef]
- Pulz, O.; Gross, W. Valuable products from biotechnology of microalgae. Appl. Microbiol. Biotechnol. 2004, 65, 635–648. [Google Scholar] [CrossRef] [PubMed]
- Spínola, M.P.; Costa, M.M.; Prates, J.A.M. Enhancing Digestibility of Chlorella vulgaris Biomass in Monogastric Diets: Strategies and Insights. Animals 2023, 13, 1017. [Google Scholar] [CrossRef]
- Wild, K.J.; Steingaß, H.; Rodehutscord, M. Variability in nutrient composition and in vitro crude protein digestibility of 16 microalgae products. J. Anim. Physiol. Anim. Nutr. 2018, 102, 1306–1319. [Google Scholar] [CrossRef]
- Spínola, M.P.; Costa, M.M.; Prates, J.A.M. Studies on the Impact of Selected Pretreatments on Protein Solubility of Arthrospira platensis Microalga. Agriculture 2023, 13, 221. [Google Scholar] [CrossRef]
- Coelho, D.; Lopes, P.A.; Cardoso, V.; Ponte, P.; Brás, J.; Madeira, M.S.; Alfaia, C.M.; Bandarra, N.M.; Fontes, C.M.; Prates, J.A. A two-enzyme constituted mixture to improve the degradation of Arthrospira platensis microalga cell wall for monogastric diets. J. Anim. Physiol. Anim. Nutr. 2020, 104, 310–321. [Google Scholar] [CrossRef]
- MišurCoVá, L.; KráčMar, S.; KLeJduS, B.; VaCeK, J. Nitrogen content, dietary fiber, and digestibility in algal food products. Czech J. Food Sci. 2010, 28, 27–35. [Google Scholar] [CrossRef]
- Niccolai, A.; Zittelli, G.C.; Rodolfi, L.; Biondi, N.; Tredici, M.R. Microalgae of interest as food source: Biochemical composition and digestibility. Algal Res. 2019, 42, 101617. [Google Scholar] [CrossRef]
- Costa, M.M.; Spínola, M.P.; Prates, J.A.M. Combination of Mechanical/Physical Pretreatments with Trypsin or Pancreatin on Arthrospira platensis Protein Degradation. Agriculture 2023, 13, 198. [Google Scholar] [CrossRef]
- Canelli, G.; Martínez, P.M.; Hauser, B.M.; Kuster, I.; Rohfritsch, Z.; Dionisi, F.; Bolten, C.J.; Neutsch, L.; Mathys, A. Tailored enzymatic treatment of Chlorella vulgaris cell wall leads to effective disruption while preserving oxidative stability. LWT 2021, 143, 111157. [Google Scholar] [CrossRef]
- Gille, A.; Trautmann, A.; Posten, C.; Briviba, K. Bioaccessibility of carotenoids from Chlorella vulgaris and Chlamydomonas reinhardtii. Int. J. Food Sci. Nutr. 2016, 67, 507–513. [Google Scholar] [CrossRef] [PubMed]
- Safi, C.; Charton, M.; Ursu, A.; Laroche, C.; Zebib, B.; Pontalier, P.; Vaca-Garcia, C. Release of hydro-soluble microalgal proteins using mechanical and chemical treatments. Algal Res. 2014, 3, 55–60. [Google Scholar] [CrossRef]
- Spínola, M.P.; Costa, M.M.; Prates, J.A.M. Effect of Selected Mechanical/Physical Pre-Treatments on Chlorella vulgaris Protein Solubility. Agriculture 2023, 13, 1309. [Google Scholar] [CrossRef]
- Coelho, D.; Lopes, P.A.; Cardoso, V.; Ponte, P.; Brás, J.; Madeira, M.S.; Alfaia, C.M.; Bandarra, N.M.; Gerken, H.G.; Fontes, C.M. Novel combination of feed enzymes to improve the degradation of Chlorella vulgaris recalcitrant cell wall. Sci. Rep. 2019, 9, 5382. [Google Scholar] [CrossRef]
- Kose, A.; Ozen, M.O.; Elibol, M.; Oncel, S.S. Investigation of in vitro digestibility of dietary microalga Chlorella vulgaris and cyanobacterium Spirulina platensis as a nutritional supplement. 3 Biotech 2017, 7, 170. [Google Scholar] [CrossRef]
- Christaki, E.; Florou-Paneri, P.; Bonos, E. Microalgae: A novel ingredient in nutrition. Int. J. Food Sci. Nutr. 2011, 62, 794–799. [Google Scholar] [CrossRef]
- Priyadarshani, I.; Rath, B. Commercial and industrial applications of micro algae—A review. J. Algal Biomass Util. 2012, 3, 89–100. [Google Scholar]
- Wan, M. Techniques for Enhancing the Digestibility of Microalgal Protein: A Review. Algal Res. 2019, 41, 101555. [Google Scholar]
- Altmann, B.A.; Neumann, C.; Rothstein, S.; Liebert, F.; Mörlein, D. Do dietary soy alternatives lead to pork quality improvements or drawbacks? A look into micro-alga and insect protein in swine diets. Meat Sci. 2019, 153, 26–34. [Google Scholar] [CrossRef] [PubMed]
- Aouir, A.; Amiali, M.; Bitam, A.; Benchabane, A.; Raghavan, V.G. Comparison of the biochemical composition of different Arthrospira platensis strains from Algeria, Chad and the USA. J. Food Meas. Charact. 2017, 11, 913–923. [Google Scholar] [CrossRef]
- Assaye, H.; Belay, A.; Desse, G.; Gray, D. Seasonal variation in the nutrient profile of Arthrospira fusiformis biomass harvested from an Ethiopian soda lake, Lake Chitu. J. Appl. Phycol. 2018, 30, 1597–1606. [Google Scholar] [CrossRef]
- Assunção, M.F.; Varejão, J.M.; Santos, L.M. Nutritional characterization of the microalga Ruttnera lamellosa compared to Porphyridium purpureum. Algal Res. 2017, 26, 8–14. [Google Scholar] [CrossRef]
- Batista, A.P.; Gouveia, L.; Bandarra, N.M.; Franco, J.M.; Raymundo, A. Comparison of microalgal biomass profiles as novel functional ingredient for food products. Algal Res. 2013, 2, 164–173. [Google Scholar] [CrossRef]
- Batista, A.P.; Niccolai, A.; Fradinho, P.; Fragoso, S.; Bursic, I.; Rodolfi, L.; Biondi, N.; Tredici, M.R.; Sousa, I.; Raymundo, A. Microalgae biomass as an alternative ingredient in cookies: Sensory, physical and chemical properties, antioxidant activity and in vitro digestibility. Algal Res. 2017, 26, 161–171. [Google Scholar] [CrossRef]
- Bélanger, A.; Sarker, P.K.; Bureau, D.P.; Chouinard, Y.; Vandenberg, G.W. Apparent digestibility of macronutrients and fatty acids from microalgae (Schizochytrium sp.) fed to rainbow trout (Oncorhynchus mykiss): A potential candidate for fish oil substitution. Animals 2021, 11, 456. [Google Scholar] [CrossRef]
- Bensehaila, S.; Doumandji, A.; Boutekrabt, L.; Manafikhi, H.; Peluso, I.; Bensehaila, K.; Kouache, A.; Bensehaila, A. The nutritional quality of Spirulina platensis of Tamenrasset, Algeria. Afr. J. Biotechnol. 2015, 14, 1649–1654. [Google Scholar]
- Bertoldi, F.C.; Sant’Anna, E.; Oliveira, J.L.B. Chlorophyll content and minerals profile in the microalgae Chlorella vulgaris cultivated in hydroponic wastewater. Ciência Rural 2008, 38, 54–58. [Google Scholar] [CrossRef]
- Cabrita, A.R.; Guilherme-Fernandes, J.; Valente, I.M.; Almeida, A.; Lima, S.A.; Fonseca, A.J.; Maia, M.R. Nutritional composition and untargeted metabolomics reveal the potential of Tetradesmus obliquus, Chlorella vulgaris and Nannochloropsis oceanica as valuable nutrient sources for dogs. Animals 2022, 12, 2643. [Google Scholar] [CrossRef] [PubMed]
- Cabrol, M.B.; Martins, J.C.; Malhão, L.P.; Alfaia, C.M.; Prates, J.A.; Almeida, A.M.; Lordelo, M.; Raymundo, A. Digestibility of meat mineral and proteins from broilers fed with graded levels of Chlorella vulgaris. Foods 2022, 11, 1345. [Google Scholar] [CrossRef] [PubMed]
- Cerri, R.; Niccolai, A.; Cardinaletti, G.; Tulli, F.; Mina, F.; Daniso, E.; Bongiorno, T.; Zittelli, G.C.; Biondi, N.; Tredici, M. Chemical composition and apparent digestibility of a panel of dried microalgae and cyanobacteria biomasses in rainbow trout (Oncorhynchus mykiss). Aquaculture 2021, 544, 737075. [Google Scholar] [CrossRef]
- Coelho, D.; Pestana, J.; Almeida, J.M.; Alfaia, C.M.; Fontes, C.M.; Moreira, O.; Prates, J.A. A high dietary incorporation level of Chlorella vulgaris improves the nutritional value of pork fat without impairing the performance of finishing pigs. Animals 2020, 10, 2384. [Google Scholar] [CrossRef] [PubMed]
- Coelho, D.F.M.; Alfaia, C.M.R.P.M.; Assunção, J.M.P.; Costa, M.; Pinto, R.M.A.; de Andrade Fontes, C.M.G.; Lordelo, M.M.; Prates, J.A.M. Impact of dietary Chlorella vulgaris and carbohydrate-active enzymes incorporation on plasma metabolites and liver lipid composition of broilers. BMC Vet. Res. 2021, 17, 229. [Google Scholar] [CrossRef] [PubMed]
- Dalle Zotte, A.; Cullere, M.; Sartori, A.; Szendrő, Z.; Kovàcs, M.; Giaccone, V.; Dal Bosco, A. Dietary Spirulina (Arthrospira platensis) and Thyme (Thymus vulgaris) supplementation to growing rabbits: Effects on raw and cooked meat quality, nutrient true retention and oxidative stability. Meat Sci. 2014, 98, 94–103. [Google Scholar] [CrossRef] [PubMed]
- Di Lena, G.; Casini, I.; Lucarini, M.; Sanchez del Pulgar, J.; Aguzzi, A.; Caproni, R.; Gabrielli, P.; Lombardi-Boccia, G. Chemical characterization and nutritional evaluation of microalgal biomass from large-scale production: A comparative study of five species. Eur. Food Res. Technol. 2020, 246, 323–332. [Google Scholar] [CrossRef]
- Ferreira, G.F.; Pinto, L.F.R.; Maciel Filho, R.; Fregolente, L.V. Effects of cultivation conditions on Chlorella vulgaris and Desmodesmus sp. grown in sugarcane agro-industry residues. Bioresour. Technol. 2021, 342, 125949. [Google Scholar] [CrossRef]
- Fidalgo, J.; Cid, A.; Torres, E.; Sukenik, A.; Herrero, C. Effects of nitrogen source and growth phase on proximate biochemical composition, lipid classes and fatty acid profile of the marine microalga Isochrysis galbana. Aquaculture 1998, 166, 105–116. [Google Scholar] [CrossRef]
- Fuentes, M.R.; Fernández, G.A.; Pérez, J.S.; Guerrero, J.G. Biomass nutrient profiles of the microalga Porphyridium cruentum. Food Chem. 2000, 70, 345–353. [Google Scholar] [CrossRef]
- Fuentes, M.R.; Fernández, G.A.; Pérez, J.S.; Gil García, M.D.; Guerrero, J.G. Nutrient composition of the biomass of the microalga Porphyridium cruentum. Food Sci. Tech. Int. 2000, 6, 129–135. [Google Scholar] [CrossRef]
- Gamboa-Delgado, J.; Morales-Navarro, Y.I.; Nieto-López, M.G.; Villarreal-Cavazos, D.A.; Cruz-Suárez, L.E. Assimilation of dietary nitrogen supplied by fish meal and microalgal biomass from Spirulina (Arthrospira platensis) and Nannochloropsis oculata in shrimp Litopenaeus vannamei fed compound diets. J. Appl. Phycol. 2019, 31, 2379–2389. [Google Scholar] [CrossRef]
- Habte-Tsion, H.-M.; Kolimadu, G.D.; Rossi, W., Jr.; Filer, K.; Kumar, V. Effects of Schizochytrium and micro-minerals on immune, antioxidant, inflammatory and lipid-metabolism status of Micropterus salmoides fed high-and low-fishmeal diets. Sci. Rep. 2020, 10, 7457. [Google Scholar] [CrossRef] [PubMed]
- Hadley, K.; Bauer, J.; Milgram, N. The oil-rich alga Schizochytrium sp. as a dietary source of docosahexaenoic acid improves shape discrimination learning associated with visual processing in a canine model of senescence. Prostaglandins Leukot. Essent. Fat. Acids 2017, 118, 10–18. [Google Scholar] [CrossRef] [PubMed]
- Holman, B.; Kashani, A.; Malau-Aduli, A. Effects of Spirulina (Arthrospira platensis) supplementation level and basal diet on live weight, body conformation and growth traits in genetically divergent Australian dual-purpose lambs during simulated drought and typical pasture grazing. Small Rumin. Res. 2014, 120, 6–14. [Google Scholar] [CrossRef]
- Holman, B.; Malau-Aduli, A. Spirulina as a livestock supplement and animal feed. J. Anim. Physiol. Anim. Nutr. 2013, 97, 615–623. [Google Scholar] [CrossRef] [PubMed]
- Karapanagiotidis, I.; Metsoviti, M.; Gkalogianni, E.; Psofakis, P.; Asimaki, A.; Katsoulas, N.; Papapolymerou, G.; Zarkadas, I. The effects of replacing fishmeal by Chlorella vulgaris and fish oil by Schizochytrium sp. and Microchloropsis gaditana blend on growth performance, feed efficiency, muscle fatty acid composition and liver histology of gilthead seabream (Sparus aurata). Aquaculture 2022, 561, 738709. [Google Scholar] [CrossRef]
- Kousoulaki, K.; Mørkøre, T.; Nengas, I.; Berge, R.; Sweetman, J. Microalgae and organic minerals enhance lipid retention efficiency and fillet quality in Atlantic salmon (Salmo salar L.). Aquaculture 2016, 451, 47–57. [Google Scholar] [CrossRef]
- Ludevese-Pascual, G.; Dela Peña, M.; Tornalejo, J. Biomass production, proximate composition and fatty acid profile of the local marine thraustochytrid isolate, Schizochytrium sp. LEY 7 using low-cost substrates at optimum culture conditions. Aquac. Res. 2016, 47, 318–328. [Google Scholar] [CrossRef]
- Macias-Sancho, J.; Poersch, L.H.; Bauer, W.; Romano, L.A.; Wasielesky, W.; Tesser, M.B. Fishmeal substitution with Arthrospira (Spirulina platensis) in a practical diet for Litopenaeus vannamei: Effects on growth and immunological parameters. Aquaculture 2014, 426, 120–125. [Google Scholar] [CrossRef]
- Madhubalaji, C.; Mudaliar, S.N.; Chauhan, V.S.; Sarada, R. Evaluation of drying methods on nutritional constituents and antioxidant activities of Chlorella vulgaris cultivated in an outdoor open raceway pond. J. Appl. Phycol. 2021, 33, 1419–1434. [Google Scholar] [CrossRef]
- Martins, C.F.; Ribeiro, D.M.; Costa, M.; Coelho, D.; Alfaia, C.M.; Lordelo, M.; Almeida, A.M.; Freire, J.P.; Prates, J.A. Using microalgae as a sustainable feed resource to enhance quality and nutritional value of pork and poultry meat. Foods 2021, 10, 2933. [Google Scholar] [CrossRef]
- Michael, A.; Kyewalyanga, M.S.; Lugomela, C.V. Biomass and nutritive value of Spirulina (Arthrospira fusiformis) cultivated in a cost-effective medium. Ann. Microbiol. 2019, 69, 1387–1395. [Google Scholar] [CrossRef]
- Neylan, K.A.; Johnson, R.B.; Barrows, F.T.; Marancik, D.P.; Hamilton, S.L.; Gardner, L.D. Evaluating a microalga (Schizochytrium sp.) as an alternative to fish oil in fish-free feeds for sablefish (Anoplopoma fimbria). Aquaculture 2024, 578, 740000. [Google Scholar] [CrossRef]
- Oliveira, E.G.d.; Rosa, G.S.d.; Moraes, M.A.d.; Pinto, L.A.d.A. Characterization of thin layer drying of Spirulina platensis utilizing perpendicular air flow. Bioresour. Technol. 2009, 100, 1297–1303. [Google Scholar] [CrossRef]
- Panahi, Y.; Pishgoo, B.; Jalalian, H.R.; Mohammadi, E.; Taghipour, H.R.; Sahebkar, A.; Abolhasani, E. Investigation of the effects of Chlorella vulgaris as an adjunctive therapy for dyslipidemia: Results of a randomised open-label clinical trial. Nutr. Diet. 2012, 69, 13–19. [Google Scholar] [CrossRef]
- Prabakaran, G.; Moovendhan, M.; Arumugam, A.; Matharasi, A.; Dineshkumar, R.; Sampathkumar, P. Evaluation of chemical composition and in vitro anti-inflammatory effect of marine microalgae Chlorella vulgaris. Waste Biomass Valorization 2019, 10, 3263–3270. [Google Scholar] [CrossRef]
- Radhakrishnan, S.; Belal, I.E.; Seenivasan, C.; Muralisankar, T.; Bhavan, P.S. Impact of fishmeal replacement with Arthrospira platensis on growth performance, body composition and digestive enzyme activities of the freshwater prawn, Macrobrachium rosenbergii. Aquac. Rep. 2016, 3, 35–44. [Google Scholar] [CrossRef]
- Rohani-Ghadikolaei, K.; Ng, W.K.; Abdulalian, E.; Naser, A.; Yusuf, A. The effect of seaweed extracts, as a supplement or alternative culture medium, on the growth rate and biochemical composition of the microalga, I sochrysis galbana (Park 1949). Aquac. Res. 2012, 43, 1487–1498. [Google Scholar] [CrossRef]
- Sathyamoorthy, G.; Rajendran, T. Growth and biochemical profiling of marine microalgae Chlorella salina with response to nitrogen starvation. Mar. Biol. Res. 2022, 18, 307–314. [Google Scholar] [CrossRef]
- Shaaban, M.M.; El-Saady, A.K.M.; El-Sayed, A.B. Green microalgae water extract and micronutrients foliar application as promoters to nutrient balance and growth of wheat plants. J. Am. Sci. 2010, 6, 631–636. [Google Scholar]
- Shabana, E.F.; Gabr, M.A.; Moussa, H.R.; El-Shaer, E.A.; Ismaiel, M.M. Biochemical composition and antioxidant activities of Arthrospira (Spirulina) platensis in response to gamma irradiation. Food Chem. 2017, 214, 550–555. [Google Scholar] [CrossRef] [PubMed]
- Shields, R.; Lupatsch, I. Algae for aquaculture and animal feeds. TATuP-Z. Für Tech. Theor. Prax. 2012, 21, 23–37. [Google Scholar]
- Sucu, E. Effects of microalgae species on in vitro rumen fermentation pattern and methane production. Ann. Anim. Sci. 2020, 20, 207–218. [Google Scholar] [CrossRef]
- Thomas, W.; Seibert, D.; Alden, M.; Neori, A.; Eldridge, P. Yields, photosynthetic efficiencies and proximate composition of dense marine microalgal cultures. III. Isochrysis sp. and Monallantus salina experiments and comparative conclusions. Biomass 1984, 5, 299–316. [Google Scholar] [CrossRef]
- Tibbetts, S.M.; MacPherson, M.J.; Park, K.C.; Melanson, R.J.; Patelakis, S.J. Composition and apparent digestibility coefficients of essential nutrients and energy of cyanobacterium meal produced from Spirulina (Arthrospira platensis) for freshwater-phase Atlantic salmon (Salmo salar L.) pre-smolts. Algal Res. 2023, 70, 103017. [Google Scholar] [CrossRef]
- Tibbetts, S.M.; Milley, J.E.; Lall, S.P. Chemical composition and nutritional properties of freshwater and marine microalgal biomass cultured in photobioreactors. J. Appl. Phycol. 2015, 27, 1109–1119. [Google Scholar] [CrossRef]
- Tokuşoglu, Ö.; Üunal, M. Biomass nutrient profiles of three microalgae: Spirulina platensis, Chlorella vulgaris, and Isochrisis galbana. J. Food Sci. 2003, 68, 1144–1148. [Google Scholar] [CrossRef]
- Kalia, S.; Lei, X.G. Dietary microalgae on poultry meat and eggs: Explained versus unexplained effects. Curr. Opin. Biotechnol. 2022, 75, 102689. [Google Scholar] [CrossRef]
- Toyomizu, M.; Sato, K.; Taroda, H.; Kato, T.; Akiba, Y. Effects of dietary spirulina on meat colour in the muscle of broiler chickens. Br. Poult. Sci. 2001, 42, 197–202. [Google Scholar] [CrossRef]
- Bonos, E.; Kasapidou, E.; Kargopoulos, A.; Karampampas, A.; Nikolakakis, I.; Christaki, E.; Florou-Paneri, P. Spirulina as a functional ingredient in broiler chicken diets. S. Afr. J. Anim. Sci. 2016, 46, 94–102. [Google Scholar] [CrossRef]
- Zahroojian, N.; Moravej, H.; Shivazad, M. Effects of dietary marine algae (Spirulina platensis) on egg quality and production performance of laying hens. J. Agric. Sci. Technol. 2013, 15, 1353–1360. [Google Scholar]
- Evans, A.; Smith, D.; Moritz, J. Effects of algae incorporation into broiler starter diet formulations on nutrient digestibility and 3 to 21 d bird performance. J. Appl. Poult. Res. 2015, 24, 206–214. [Google Scholar] [CrossRef]
- Shanmugapriya, B.; Babu, S.S.; Hariharan, T.; Sivaneswaran, S.; Anusha, M. Dietary administration of Spirulina platensis as probiotics on growth performance and histopathology in broiler chicks. Int. J. Recent Sci. Res. 2015, 6, 2650–2653. [Google Scholar]
- Abbas, A.O.; Alaqil, A.A.; Mehaisen, G.M.K.; Kamel, N.N. Effect of Dietary Blue-Green Microalgae Inclusion as a Replacement to Soybean Meal on Laying Hens’ Performance, Egg Quality, Plasma Metabolites, and Hematology. Animals 2022, 12, 2816. [Google Scholar] [PubMed]
- Pestana, J.M.; Puerta, B.; Santos, H.; Madeira, M.S.; Alfaia, C.M.; Lopes, P.A.; Pinto, R.M.A.; Lemos, J.P.C.; Fontes, C.M.G.A.; Lordelo, M.M.; et al. Impact of dietary incorporation of Spirulina (Arthrospira platensis) and exogenous enzymes on broiler performance, carcass traits, and meat quality. Poult. Sci. 2020, 99, 2519–2532. [Google Scholar] [CrossRef] [PubMed]
- El-Hady, A.M.A.; Elghalid, O.A.; Elnaggar, A.S.; El-khalek, E.A. Growth performance and physiological status evaluation of Spirulina platensis algae supplementation in broiler chicken diet. Livest. Sci. 2022, 263, 105009. [Google Scholar] [CrossRef]
- Dlouhá, G.; Sevcikova, S.; Dokoupilova, A.; Zita, L.; Heindl, J.; Skrivan, M. Effect of dietary selenium sources on growth performance, breast muscle selenium, glutathione peroxidase activity and oxidative stability in broilers. Czech J. Anim. Sci. 2008, 53, 265. [Google Scholar] [CrossRef]
- Kang, H.; Salim, H.; Akter, N.; Kim, D.; Kim, J.; Bang, H.; Kim, M.; Na, J.; Hwangbo, J.; Choi, H. Effect of various forms of dietary Chlorella supplementation on growth performance, immune characteristics, and intestinal microflora population of broiler chickens. J. Appl. Poult. Res. 2013, 22, 100–108. [Google Scholar] [CrossRef]
- Oh, S.T.; Zheng, L.; Kwon, H.; Choo, Y.; Lee, K.; Kang, C.; An, B.-K. Effects of dietary fermented Chlorella vulgaris (CBT®) on growth performance, relative organ weights, cecal microflora, tibia bone characteristics, and meat qualities in Pekin ducks. Asian-Australas. J. Anim. Sci. 2015, 28, 95. [Google Scholar] [CrossRef]
- Englmaierová, M.; Skrivan, M.; Bubancová, I. A comparison of lutein, spray-dried Chlorella, and synthetic carotenoids effects on yolk colour, oxidative stability, and reproductive performance of laying hens. Czech J. Anim. Sci. 2013, 58, 412–419. [Google Scholar] [CrossRef]
- Alfaia, C.M.; Pestana, J.M.; Rodrigues, M.; Coelho, D.; Aires, M.J.; Ribeiro, D.M.; Major, V.T.; Martins, C.F.; Santos, H.; Lopes, P.A.; et al. Influence of dietary Chlorella vulgaris and carbohydrate-active enzymes on growth performance, meat quality and lipid composition of broiler chickens. Poult. Sci. 2021, 100, 926–937. [Google Scholar] [CrossRef] [PubMed]
- Ginzberg, A.; Cohen, M.; Sod-Moriah, U.A.; Shany, S.; Rosenshtrauch, A.; Arad, S. Chickens fed with biomass of the red microalga Porphyridium sp. have reduced blood cholesterol level and modified fatty acid composition in egg yolk. J. Appl. Phycol. 2000, 12, 325–330. [Google Scholar] [CrossRef]
- Yan, L.; Kim, I. Effects of dietary ω-3 fatty acid-enriched microalgae supplementation on growth performance, blood profiles, meat quality, and fatty acid composition of meat in broilers. J. Appl. Anim. Res. 2013, 41, 392–397. [Google Scholar] [CrossRef]
- Ribeiro, T.; Lordelo, M.M.; Alves, S.P.; Bessa, R.J.; Costa, P.; Lemos, J.P.; Ferreira, L.M.; Fontes, C.M.; Prates, J.A. Direct supplementation of diet is the most efficient way of enriching broiler meat with n-3 long-chain polyunsaturated fatty acids. Br. Poult. Sci. 2013, 54, 753–765. [Google Scholar] [CrossRef]
- Ribeiro, T.; Lordelo, M.M.; Costa, P.; Alves, S.P.; Benevides, W.S.; Bessa, R.J.; Lemos, J.P.; Pinto, R.M.; Ferreira, L.M.; Fontes, C.M.; et al. Effect of reduced dietary protein and supplementation with a docosahexaenoic acid product on broiler performance and meat quality. Br. Poult. Sci. 2014, 55, 752–765. [Google Scholar] [CrossRef] [PubMed]
- Pittman, J.K.; Dean, A.P.; Osundeko, O. The potential of sustainable algal biofuel production using wastewater resources. Bioresour. Technol. 2011, 102, 17–25. [Google Scholar] [CrossRef] [PubMed]
- Lam, M.K.; Lee, K.T. Microalgae biofuels: A critical review of issues, problems and the way forward. Biotechnol. Adv. 2012, 30, 673–690. [Google Scholar] [CrossRef]
- Chisti, Y. Biodiesel from microalgae. Biotechnol. Adv. 2007, 25, 294–306. [Google Scholar] [CrossRef]
- Clarens, A.F.; Resurreccion, E.P.; White, M.A.; Colosi, L.M. Environmental Life Cycle Comparison of Algae to Other Bioenergy Feedstocks. Environ. Sci. Technol. 2010, 44, 1813–1819. [Google Scholar] [CrossRef]
- Stephens, E. Lifecycle Assessment of Algae Biofuel Production: A Critical Review. Energy Environ. Sci. 2010, 3, 605–621. [Google Scholar]
- Ahmad, A.; Ashraf, S.S. Sustainable food and feed sources from microalgae: Food security and the circular bioeconomy. Algal Res. 2023, 74, 103185. [Google Scholar] [CrossRef]
- Brennan, L.; Owende, P. Biofuels from microalgae—A review of technologies for production, processing, and extractions of biofuels and co-products. Renew. Sustain. Energy Rev. 2010, 14, 557–577. [Google Scholar] [CrossRef]
- Grima, E.M.; Belarbi, E.-H.; Fernández, F.A.; Medina, A.R.; Chisti, Y. Recovery of microalgal biomass and metabolites: Process options and economics. Biotechnol. Adv. 2003, 20, 491–515. [Google Scholar] [CrossRef] [PubMed]
- Slade, R.; Bauen, A. Micro-algae cultivation for biofuels: Cost, energy balance, environmental impacts and future prospects. Biomass Bioenergy 2013, 53, 29–38. [Google Scholar] [CrossRef]
- Carmichael, W.W. Health effects of toxin-producing cyanobacteria: “The CyanoHABs”. Hum. Ecol. Risk Assess. Int. J. 2001, 7, 1393–1407. [Google Scholar] [CrossRef]
- Spolaore, P.; Joannis-Cassan, C.; Duran, E.; Isambert, A. Commercial applications of microalgae. J. Biosci. Bioeng. 2006, 101, 87–96. [Google Scholar] [CrossRef]
- Committee, E.S.; Hardy, A.; Benford, D.; Halldorsson, T.; Jeger, M.J.; Knutsen, H.K.; More, S.; Naegeli, H.; Noteborn, H.; Ockleford, C. Guidance on the risk assessment of substances present in food intended for infants below 16 weeks of age. EFSA J. 2017, 15, e04849. [Google Scholar]
- Smith, K. The Importance of Clear and Responsible Labeling of Animal Products Derived from Animals Fed with Microalgae. Food Control 2010, 21, 815–822. [Google Scholar]
Microalga | Dietary Inclusion and Animals | Impact | Reference |
---|---|---|---|
Arthrospira sp. | 4–8% in 21-day-old male chicks for 16 days | No significant effect on ADG | [80] |
1% in 1-day-old broiler chicks | Increased ADG and decreased FCR | [84] | |
9% in laying hens | Improved egg quality | [85] | |
15% in 1-day-old broilers | Increased total carotenoids in meat, but reduced n-3 PUFA and α-tocopherol contents | [86] | |
3 and 6% in broilers | Increased Ca and P in tibia ash | [87] | |
Chlorella sp. | 1.25% in laying hens | Decreased FCR without affecting feed intake | [91] |
10% in 1-day-old broilers for 21 days | Increased total carotenoids and a small significant increase in 18:3n-3 | [92] | |
15% in 1-day-old broilers for 21 days | Increased total carotenoids but decreased n-3 PUFA and α-tocopherol contents | ||
0.1–0.2% in 1 -day-old ducks | Increased feed intake | [90] | |
Porphyridium sp. | 5–10% in 12–13, 30-week-old chickens | Reduced ADFI without affecting body weight | [93] |
Schizochytrium JB5 | 0.1–0.2% in 2-day-old broilers for 35 days | No significant effect on ADG, ADFI, or FCR | [94] |
Schizochytrium sp. | 7.4% in 21-day-old broilers | Increased ADG and ADFI | [95,96] |
Impacts | Reference |
---|---|
Low reliance on land and freshwater resources for cultivation; Microalgae thrive in environments unsuitable for traditional agriculture. | [97] |
Microalgae sequester carbon dioxide, a crucial feature in the battle against climate change. Through the process of photosynthesis, microalgae incorporate CO2 into their biomass, effectively reducing greenhouse gas emissions. | [98] |
Microalgae assist in bioremediation and pollution control. | [99] |
Microalgae are an alternative nutrient source, potentially reducing the exploitation of natural resources and helping preserve biodiversity. | [100] |
Aspects | Reference |
---|---|
Establishing and maintaining cultivation systems can be costly; open ponds are more cost-effective; photobioreactors provide better control over growing conditions. | [103] |
Harvesting and processing can be energy-intensive and thus expensive. | [104] |
Cost-effectiveness is influenced by the bioavailability of nutrients in poultry. | [11] |
Microalgae must be competitive in terms of both nutritional content and cost. | [105] |
Aspects | Reference |
---|---|
Risk of toxin and contaminant presence; Capable of producing toxins such as microcystins; Regular monitoring and stringent quality control measures are vital. | [106] |
The potential for allergenic reactions to components of microalgae, an important consideration given the novel nature of microalgae as a feed ingredient. | [107] |
Regulatory frameworks governing the use of microalgae in animal feed vary across regions. In the European Union, microalgae intended for animal feed must comply with regulations set by the European Food Safety Authority (EFSA), and in the United States, the Food and Drug Administration (FDA) is responsible for overseeing the approval of new feed ingredients. | [108] |
Transparency in labeling and consumer information is crucial, especially for novel feed ingredients like microalgae. | [109] |
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Costa, M.M.; Spínola, M.P.; Prates, J.A.M. Microalgae as an Alternative Mineral Source in Poultry Nutrition. Vet. Sci. 2024, 11, 44. https://doi.org/10.3390/vetsci11010044
Costa MM, Spínola MP, Prates JAM. Microalgae as an Alternative Mineral Source in Poultry Nutrition. Veterinary Sciences. 2024; 11(1):44. https://doi.org/10.3390/vetsci11010044
Chicago/Turabian StyleCosta, Mónica M., Maria P. Spínola, and José A. M. Prates. 2024. "Microalgae as an Alternative Mineral Source in Poultry Nutrition" Veterinary Sciences 11, no. 1: 44. https://doi.org/10.3390/vetsci11010044
APA StyleCosta, M. M., Spínola, M. P., & Prates, J. A. M. (2024). Microalgae as an Alternative Mineral Source in Poultry Nutrition. Veterinary Sciences, 11(1), 44. https://doi.org/10.3390/vetsci11010044