Macro- and microalgae have been considered as alternative ingredients due to their high growth rates and lack of competition for arable land for cultivation. Macroalgae are multicellular and macroscopic algae, and depending on the species, their nutritional value is quite different. Because of their nutritional value, their bioactive compounds and their potential prebiotic properties, microalgae have been recognised as an interesting ingredient for fish feed, and specifically as an alternative protein source. Their high production costs have been a major obstacle to their viable inclusion in fish feeds; however, in the near future, this limitation should be overcome.
In this context, this synthesis aims to review the impacts of these potential alternative and novel dietary protein sources on stress, immune responses, health and disease resistance in fish.
Impact of alternative protein sources on intestinal and liver health in fish
Soya was considered a good alternative to fishmeal due to its high protein content, relatively balanced amino acid profile and availability. However, studies have shown that dietary inclusion of soybean meal at levels above 10% induced enteritis in fish. The disorder was associated with the presence of anti-nutritional factors in crude soybean meal, in particular soybean saponins. The integrity of the intestinal epithelium is fundamental to the absorption of nutrients, and the negative effects of plant protein-based diets on intestinal health can lead to disturbances in intestinal absorption function. Alterations to the intestinal epithelium caused by enteritis adversely affect nutrient digestibility, the activities of intestinal enzymes and the expression of amino acid and peptide transporter genes. Consequently, disturbances in the intestinal epithelium result in reduced nutrient availability for fish, which in some circumstances can be reflected in reduced growth performance. In addition to the important role played by the intestine in the absorption of nutrients, the integrity of the intestine is essential in the defence against pathogens.
An interesting strategy with the use of innovative ingredients is their use to counter the negative effects of certain vegetable proteins. The inclusion of the microalga Chlorella vulgaris in diets containing 20% soya meal was highly effective in countering soya-induced enteropathy in Atlantic salmon. Similarly, the inclusion in the diet of a mixture of dry biomass of Tisochrysis lutea and Tetraselmis suecica improved the digestive and absorptive functions of the intestine of European sea bass, compared with fish fed a diet rich in soya meal (35% inclusion).
Thus, the strategic use of innovative ingredients, such as microalgae, can mitigate the negative effects of plant proteins in diets.
Impact of alternative protein sources on fish microbiota
The intestinal microbiota of fish plays a crucial role in their health, influencing processes such as digestion, immune defence and tissue stability. One of the most relevant processes influenced by the microbiota is the digestion of food components that are indigestible to the host, leading to the synthesis of short-chain fatty acids. These represent a major source of energy for intestinal epithelial cells and are essential for intestinal health. Microbial composition is known to vary according to species, season and life-cycle events, among other factors. The intestinal microbiota of fish is also fairly sensitive to dietary manipulation.
Alternative proteins, particularly those from algae, modulate the composition of the microbiota. However, their effectiveness is highly dependent on the inclusion rate, the species of algae and the pre-treatment of the biomass to enhance digestibility and nutrient utilisation. Algae (Ulva rigida, Schizochytrium limacinum, Arthrospira platensis) incorporated into feed at a rate of 5 to 25% seem promising, reducing the abundance of potentially pathogenic flora and increasing that of beneficial bacteria such as Lactobacillus. This modulation of the microbiota could contribute to greater resistance to disease, lower mortality and better performance in fish fed on algae. In vitro studies did not reveal any direct inhibitory effect against the pathogen, highlighting that the result is probably due to the prebiotic capacities of the algae; the reduction in pathogen abundance is an indirect effect of the modulation of the microbial network. More studies are needed to address this potential disease resistance with algal modulation of the microbiota, linking microbiota abundance to physiological outcomes.
Impact of alternative protein sources on immune function and disease resistance
The activation of the immune system in fish leads to specific nutritional requirements, influencing the competition between nutrients for maintenance, immune function and the deposition of body proteins. Nutrition can therefore have significant implications for fish health.
Macro and microalgae provide essential and bioactive nutrients to farmed fish. Several species have been studied as natural sources for improving innate immunity, such as Ulva rigida, Gracilaria gracilis and Arthrospira platensis, among others.
Algae have shown beneficial effects, positively modulating immune parameters and improving resistance to pathogens in various fish species. Microalgae such as Tetraselmis sp. and Chlorella sp. were associated with increased immune activity in gilthead seabream, while spirulina (Arthrospira platensis) improved survival and immune responses in European sea bass. The results varied according to the source of algae, the species of fish and the inclusion conditions (2.5% to 25%). Further studies are needed to determine the best inclusion rates, the effects on different fish species and the underlying mechanisms for optimising the use of algae in fish feed in aquaculture.
Impact of alternative protein sources on stress response
Fish respond to stress through a complex cascade of neurological and physiological processes, resulting in energy-intensive trade-offs that can affect growth and immunocompetence. Dietary modulation of the stress response is well studied, and dietary protein plays a major role in how fish respond to challenges. Functional additives, such as probiotics and prebiotics, are often studied for their stress-mitigating properties. Algae, as an alternative source of protein with a rich bioactive composition, are also considered to be stress-mitigating ingredients. Studies have shown that the inclusion of microalgae such as spirulina (5% to 28%) and Tetraselmis sp. (10%) or macroalgae such as Sargassum aquifolium (20%) in fish feed can reduce plasma glucose and cortisol levels after stressful events. Certain bioactive compounds in algae, such as antioxidants, phlorotannins and fucoidans, can help improve fish resistance to stress. However, the effects depend on the source of algae, the species of fish and the dose of inclusion, underlining the need for in-depth research into precise nutrition adapted to the specific needs of fish.
Impacts des sources de protéines alternatives sur le stress oxydatif
Oxidative stress can have adverse effects on the health, performance and flesh quality of farmed fish, underlining the importance of maintaining an optimal redox balance. Nutrition plays a crucial role in modulating oxidative stress, with diets balanced in antioxidant compounds promoting animal allostasis. However, certain food ingredients can induce oxidative stress due to the presence of anti-nutritional factors, amino acid deficiencies or an excess of proteins/lipids. Including microalgae in fish feed could help reduce oxidative stress. A 19% inclusion of Arthrospira platensis or Chlorella vulgaris in the diets of African catfish (Clarias gariepinus) may enhance growth performance and increase the activity of the antioxidants SOD and CAT in these fish, compared with those fed a diet without microalgae. The results suggest that the use of innovative ingredients, such as algae, may be a valuable option for replacing fishmeal without compromising the growth performance or robustness of the fish.
In conclusion, aquaculture has emerged as a major player in animal protein production. This growth is inextricably linked to advances in fish nutrition, with fishmeal playing a central role due to its exceptional nutritional properties.
However, sustainability concerns have spurred the search for alternatives to fishmeal. Alternative sources, such as vegetable ingredients, processed animal by-products, microalgae, proteins from single-celled organisms, macroalgae and insects, are being studied to minimise the environmental, economic and social impact.
Macro- and microalgae are emerging as promising alternatives because of their high productivity and their potential to use no arable land. However, their high production costs are still a challenge to overcome.
Algae are emerging as viable options for feeding fish in aquaculture, offering potential benefits for sustainability, gut health, disease resistance, stress response and modulation of oxidative stress. However, further research is needed to optimise inclusion rates, understand the underlying mechanisms and ensure accurate nutrition tailored to the specific needs of different fish species.
Aragão, C.; Gonçalves, A.T.; Costas, B.; Azeredo, R.; Xavier, M.J.; Engrola, S. Alternative Proteins for Fish Diets: Implications beyond Growth. Animals 2022, 12, 1211. https://doi.org/10.3390/ani12091211