General proximate composition and energy content of various genera of microalgae evaluated for use in salmonid feeds (dry weight basis).
Abstract
Microalgae-based ingredients have potential to ensure continued growth of salmonid aquaculture for global sustainable food security in the blue economy. Algal biorefineries must valorize the entire crop to grow profitable microalgae-based economies. With massive growth and demand for novel sustainable ingredients, farmed salmonid feed sectors are highly promising areas to focus on. Microalgae-based ingredients for salmonid feeds may have market advantages in terms of lower input costs, aerial foot-print, wastewater remediation benefits and carbon credits for industrial CO2 conversion. A handful of microalgae-based ingredients have been proposed as candidates to supply well-balanced nutrients and immunostimulatory compounds. However, technical gaps exist and need addressing before the industry could economically incorporate microalgae-based ingredients into commercial feeds. Current knowledge on comprehensive biochemical composition is incomplete, highly heterogeneous, and information on their nutritional value is scattered and/or inconsistent. The aim of this chapter is to consolidate relatively fragmented data on biochemical composition and nutritional value of microalgae-based ingredients focusing on farmed salmonid feeds. Presented are discussions on the potential for such ‘next-generation’ ingredients, opportunities/challenges for their use and a compendium of studies evaluating their performance in feeds for economically relevant farmed salmonids, including rainbow trout (Oncorhynchus mykiss), Arctic charr (Salvelinus alpinus) and Atlantic salmon (Salmo salar).
Keywords
- microalgae
- salmonids
- aquaculture feeds
- composition
- nutritional value
1. Importance of aquaculture in the blue revolution
Most developed countries are nearing their terrestrial agricultural output capacity. Terrestrial agriculture will be highly challenged to meet the demands for a growing human population. Food production requires an epic shift towards leveraging intrinsic competitive advantages from our aquatic environment. As such, we have now entered the blue revolution where dietary protein and essential nutrients are increasingly derived from aquatic environments. However, most traditional capture fisheries are depleted or harvested at their biological limits. As stated a half century ago by famous marine explorer and ecologist Jacques Cousteau “We must farm the sea” in order to foster strong global food security. This was reiterated in 2012 by former UN Secretary General Kofi Annan who stated “Aquaculture is crucial for supplying the world’s food needs for the next 50 years”. Recently, aquaculture has grown annually at 7.8%; far exceeding that of terrestrial farming systems like poultry (4.6%), pork (2.2%), dairy (1.4%), beef (1.0%) and grains (1.4%) [1]. As the appetite for seafoods outpaces what capture fisheries can supply, global farmed seafood supplies in 2009 matched wild-caught seafood and this proportion is projected to rise to 62% of all seafood supplies by 2030. This firmly secures aquaculture’s position in the blue economy as the most efficient use of resources for global food production. Gentry et al. [2] reported that a small fraction of coastal ocean waters (0.015%), about the size of Lake Michigan, specifically selected for sustainable aquaculture (excluding areas that interfere with shipping lanes, ocean oil extraction or marine protected areas) is required to exceed current demand for seafood by 100-fold. For the first time in history, global aquaculture production exceeded beef production in 2011 and in 2014 farmed aquatic production was valued at $160 billion USD (74 million metric tons [mmt]) and will exceed $240 billion USD by 2022. Indeed, as global economist and Nobel Laureate Dr. Peter Drucker recently stated “Aquaculture, not the internet, represents the most promising investment opportunity of the 21st century”.
2. Formulated compound aquaculture feeds
2.1. The aquafeeds dilemma
Of the 74 mmt of global farmed seafood produced annually, the majority (57 mmt or 77% of total) is from finfish and crustaceans, which are considered ‘fed’ aquaculture species. This means they require mass-produced formulated complete feeds (aquafeeds) and the production of aquafeeds will exceed 87 mmt by 2025. As a result, modern aquaculture is a major consumer of world fish meal and fish oil supplies, which has placed an unsustainable burden on traditional capture fisheries in South Pacific, South-East Asia and North Atlantic countries. This scenario represents a dramatic shift in use of these finite marine resources during the past half century. Regarding fish meal; feeds for terrestrial animals have traditionally demanded virtually all global supplies and aquafeeds consumed <1% of supply only a few decades ago, while today aquafeeds consume a staggering 73%. The situation is the same for fish oil where in 1960 virtually all supplies were used as hardened edible fats or refined industrial oils and aquafeeds used <1% of supply, while today aquafeeds consume 71%. Aside from very real ecological issues, this tremendous demand has had a direct and highly consequential economic result of tripling the cost of fish meals and oils. While farmed salmonids represent a marginal contribution (3%) to total global farmed seafood supplies, they consume a disproportionate amount of these finite resources.
2.2. Industrial farming of salmonids
Farming of salmonids (e.g., salmon, trout, charr) uses feed inputs more efficiently than terrestrial animal protein production systems (e.g., beef, poultry and pork). Typical feed conversion ratio (FCR) for salmonids is 1.2 g feed g gain−1 compared to 1.8–6.3 g feed g gain−1 for livestock. This is due to higher dietary protein and energy retention efficiency in salmonid fish (23–31%) compared to terrestrial farm animals (5–21%). Also, since fish are poikilothermic and expend less energy maintaining their position in the water column, edible yields of farmed salmonids are higher (68%) than terrestrial livestock (38–52%). Salmonid farming occupies low carbon footprints and those farmed in Norway, Chile and Canada may, in fact, be the most ecologically sustainable meat products on the global food protein market. Greenhouse gas (GHG) emissions of 2.2 kg CO2 eq. kg−1 of edible meat produced are reported in contrast to 2.7–30.0 kg CO2 eq. kg−1 for chicken, pork and beef. However, it’s important to note that salmonids are highly piscivorous and the industry remains greatly dependent upon global ocean resources; albeit to a far lower degree than previous decades. Most commercial salmonid feeds in 1995 contained ~53% fish meal, ~31% fish oil and ~16% alternative proteins and grains, while today most feeds contain ~27% fish meal, ~15% fish oil, ~43% alternative proteins and grains and ~15% alternative oils. In Norway, total dietary composition of wild marine-based ingredients has dropped from 90 to 30% between 1990 and 2013. Nevertheless, global demand for aquafeeds is less than 40 mmt but is expected to rise dramatically to 87 mmt which will continue to exacerbate the aquafeeds dilemma. Fish meal and fish oil obtained from reduction of wild-capture pelagic fish is beyond maximum sustainable limits, is becoming cost-prohibitive and could/should be better-used for direct human consumption. These wild populations may be even more pressured by global climate change and supplies will be insufficient to meet growing aquafeed demands and thus constrain aquaculture growth. This is particularly true in emerging economies like China where production accounts for 61% of global aquaculture and continues to grow rapidly.
2.3. Alternative feed ingredients—microalgae?
The aquafeeds dilemma is not new and herculean efforts were made over three decades to identify a broad range of new ingredients. This developed new commodity markets and resulted in significant industrial use of animal- and plant-based feed inputs. These include high-quality rendered animal by-products (e.g., poultry meals, hydrolyzed feather meals, meat and bone meals, blood meals, etc.) and plant-based meals and protein concentrates produced from oilseeds, grains, pulses and legumes as complete or partial replacements for fish meals. Similarly, terrestrial animal fats and plant-based oils (e.g., poultry fat, beef tallow, vegetable oils, etc.) have extensively replaced fish oil in farmed salmonid feeds. However, these ‘second-generation’ ingredients are not without limitations. Most lack certain functional properties, palatability and nutritional profiles, and many have lower digestibility and may be limited by specific antinutritional factors (ANFs) which can impair feed intake, growth performance and fish health. Some may alter final product quality for the consumer and they are also becoming increasingly costly and ecologically unsustainable. Of critical importance is that increased use of these ingredients has forced farmed salmonid production to shift alignment to terrestrial agriculture which occupies large aerial footprints, is heavily dependent on fossil fuel-based fertilizers, chemical pesticides and freshwater irrigation. Additionally, these products are grown for our own consumption; so it is of key importance to reduce competition with human food resources for sustainable production of aquafeeds. Ecological and socioeconomic issues aside, the health benefits of consuming fatty fish like farmed salmonids have become serious concerns for human nutrition with the rising use of plant-based ingredients in salmonid feeds. Uncoupling of this scenario is desperately needed to effectively minimize environmental impacts and social inequities; however, it is not simple from technological, ecological or socioeconomic viewpoints and will require economic and political incentives from governments and substantial ‘buy-in’ from industry and private investors.
3. Microalgae-based products for salmonid feeds
3.1. Opportunities
To ensure continued growth of the sustainable salmonid aquaculture sector in ways that do not deplete important terrestrial and aquatic resources, a ‘third-generation’ of feed inputs is urgently needed and it is generally agreed that they must come from lower trophic levels. Microalgae such as
3.2. Challenges
As a cautionary note, some proponents of microalgae biotechnologies suggest that they are ‘super-foods’ and feeding microalgae to farmed salmonids makes perfect sense since that is what their wild counterparts would naturally consume. This thinking encourages development of lower-trophic, ecologically-sustainable salmonid feed ingredients but the notion is, unfortunately, flawed. While it’s true many essential dietary nutrients for wild salmonids originate in aquatic phytoplankton (microalgae) and other single-celled organisms, they are delivered through ‘indirect’ passage of nutrients up the aquatic food chain and rarely via ‘direct’ intake; as salmonids do not actively seek to consume microalgae. The notion that wild, highly piscivorous salmonid fish derive nutrients from direct ingestion of microalgae is akin to the notion that wild, highly carnivorous lions derive nutrients from direct consumption of grass. On the contrary, higher trophic predators like salmonids evolved to rely on a progression of intermediary organisms (e.g., grazing phytoplankton, zooplankton, forage fish, etc.) to extract nutrients from complex food matrices that make up ‘base-of-the-food chain’ organisms (e.g., phytoplankton). This upward passage and trophic accumulation of essential nutrients, referred to as food-chain amplification, transforms them into forms that the relatively simple monogastric digestive system of salmonids can assimilate and use for productive purposes like protein synthesis, growth, tissue repair, metabolic energy and reproduction. The practical implication is that, in the absence of food-chain amplification, reliance on transformative intermediary organisms represents a nutritional barrier for direct feeding of microalgae to most monogastric animals, especially coldwater farmed salmonids. This is because their capacity to extract and utilize microalgal nutrients directly is limited by the highly recalcitrant cell walls of most microalgae, combined with the relatively short gastric (acidic) digestion phase in salmonid fishes. Some industrial downstream processing is almost certainly required in order for nutrient-rich microalgae to realize its potential as a much-needed next-generation ingredient. Like other ingredients once regarded as ‘alternatives’ but now established mainstream ingredients (e.g., corn, soy, wheat, canola, etc.), cost-effective processing technologies must be developed for microalgae to rupture cell walls, concentrate target nutrient levels, reduce/eliminate indigestible fibers, inactivate ANFs and increase nutrient digestibility for monogastric cold-water fish. With each processing step, nutritional value is increased but so is the cost of production and ultimately the market price. To further attenuate this situation, unlike terrestrial crops, microalgae cultivations must begin with dewatering the highly dilute cells (typically by centrifugation) down to a dry biomass (typically by spray-drying) and usually some means of mechanical, chemical or enzymatic cell wall rupture is required, and all these processes are currently highly energy intensive and costly. Optimizing the balance between the types and extent of downstream processing and their associated costs to determine the ‘point of diminishing returns’ that yield algal ingredients of the highest nutritional value in a cost-effective manner for least-cost salmonid ration formulations will undoubtedly occur with innovation. However, very few microalgae-based salmonid feed ingredients have yet to reach the marketplace.
3.3. Nutrient composition of microalgae in relation to their use in salmonid feeds
Beyond high production costs and relatively high prices for microalgae for aquafeeds, several broad issues must be resolved before the salmonid aquaculture feed industry can adopt microalgae-based ingredients for routine use. First, microalgae are a widely diverse class of microorganisms and many complex issues exist around their highly variable nutrient composition. This chapter is a culmination of data collected from the literature on the relevant biochemical composition of ~50 genera of microalgae from the past century. Suffice to say that the sheer size of data tables and associated >150 references preclude inclusion within the confines of this chapter. For a relatively complete compendium of biochemical composition, readers are referred to Becker [3]. Generally, proximate composition of dry microalgae is extreme for ash (<1–53%), protein (2–73%), lipid (<1–83%), carbohydrate (1–64%) and energy (4–30 MJ kg−1). This highly variable trend is predictably the same for genera that have been specifically evaluated for salmonid feeds (Table 1) for ash (1–53%), protein (3–73%), lipid (1–83%), carbohydrate (3–55%) and energy (6–30 MJ kg−1). This variability is related to the extensive biological diversity of microalgae (e.g., >100,000 documented species) and the complexities associated with their use as biological factories, large variations in cultivation strategies, variable harvesting and downstream processing methods and under-developed and inconsistent nutrient characterization analytics. Also, in contrast to agricultural crop production, large-scale algaculture is still in its embryonic stage and production tonnage needs to dramatically rise to industrial levels to realize the benefits of economies of scale that will ensure reliable supply, consistent nutrient profile, high nutrient quality and cost-competitiveness that the massive salmonid aquafeed sector will require. Lessons could be learned from the relatively niche, poorly regulated natural health food market for microalgae such as
Genera | Ash (%) | Protein (%) | Lipid (%) | Carbohydrate (%) | Energy (MJ kg−1) |
---|---|---|---|---|---|
3–13 | 42–73 | 2–16 | 8–25 | 6–23 | |
— | 43–56 | 14–22 | 3–17 | — | |
2–8 | 14–67 | 2–63 | 7–34 | 15–27 | |
4 | 15–23 | 20–56 | — | 29 | |
16 | 21–27 | 1 | — | 17 | |
1–15 | 3–48 | 7–67 | 26–55 | 24 | |
13–31 | 20–45 | 16–53 | 13–18 | — | |
53 | 12 | 3 | — | — | |
7–23 | 18–48 | 2–68 | 8–36 | 19–27 | |
16–17 | 30–49 | 7–57 | 8–25 | 20 | |
4–12 | 12–39 | 15–71 | 32–39 | 26 | |
3–14 | 8–56 | 1–58 | 10–52 | 20–23 | |
11–20 | 27–52 | 3–45 | 15–45 | 18–20 | |
8–11 | 12–21 | 8–83 | 39 | 18–30 |
3.3.1. Protein and lipid composition
Contrary to popular belief, most industrialized microalgae species do not accumulate high-value essential n-3 LC-PUFA (e.g., those in the 20 and 22 carbon chain lengths). This essential lipid deficiency may relegate these species as poor nutritional value for use in salmonid feeds when, in fact, it’s their potential for high protein accumulation that is of interest. While total protein content varies widely in the literature (often by several magnitudes) the essential amino acid (EAA) profile of that protein generally remains rather conserved among species, regardless of growth phase and/or cultivation conditions. Table 2 shows the EAA composition of microalgae genera that have been evaluated for salmonid feeds. Leucine, arginine and lysine are generally predominant in microalgal protein (on average 7 g 100 g protein−1), methionine, histidine and tryptophan are typically most limiting (on average 2 g 100 g protein−1) and isoleucine, phenylalanine, threonine and valine are mid-range (on average 4 g 100 g protein−1). An important factor when evaluating the protein quality of microalgae-based ingredients for nutrition is their concentrations of nucleic acids (RNA and DNA), which are sources of purines. It is known in primates that excessive consumption can elevate plasma uric acid, which may result in inflammatory arthritis (gout) and renal calculus (kidney stones) and this is related to the lack of digestive uricase enzyme in primates. Fortunately, farmed monogastric animals like swine, poultry and fish have different metabolic pathways which minimize accumulation of uric acid in the blood stream, such as excretion via allantoic acid, urea and ammonia. Additionally, microalgae typically contain lower levels of nucleic acids and purines (4–6%) than other single-cell proteins like yeast and bacteria (8–20%). Like other macronutrients, lipid content of microalgae varies widely and fatty acid (FA) composition is also highly heterogeneous. Table 2 shows the FA composition of microalgae genera that have been evaluated for salmonid feeds. The only discreet trend is that the lipid fraction of most species is dominated by the saturated FA (SFA) palmitic acid (16:0) and the monounsaturated FA (MUFA) oleic acid (18:1n-9); which combined generally account for about 40% of total FAs. Many marine and freshwater species, particularly
Essential amino acid (g 100 g protein−1) | ||||||||||||
Arginine | 4–8 | 3–14 | — | 6–8 | 2–6 | 6 | 2–8 | 6 | 6–7 | 1–12 | 6–9 | 7 |
Histidine | 1–5 | 1–6 | — | <1–1 | 1–3 | 1 | <1–3 | 2 | 2 | <1–3 | 1–2 | 3 |
Isoleucine | <1–7 | <1–4 | — | 2–5 | 1–5 | 4 | <1–6 | 5 | 4–5 | <1–3 | 3–4 | 4 |
Leucine | 5–14 | 3–9 | — | 5–9 | 3–9 | 7 | 5–11 | 7 | 9 | 1–6 | 7 | 8 |
Lysine | 3–8 | 2–10 | — | 4–6 | 2–6 | 7 | 3–8 | 6 | 5–6 | <1–4 | 6–7 | 6 |
Methionine | 1–5 | <1–2 | — | 1 | 1–3 | 2 | 1–3 | 3 | 2 | <1–10 | 2 | 3 |
Phenylalanine | 3–7 | 2–8 | — | 2–5 | 2–6 | 4 | 2–6 | 5 | 5–7 | <1–3 | 5 | 5 |
Threonine | 3–7 | <1–6 | — | 4–6 | 2–5 | 5 | 4–6 | 5 | 6 | 1–3 | 4–5 | 5 |
Tryptophan | <1–3 | 1–10 | — | — | 1–3 | 1 | <1–4 | 3 | <1–2 | <1–2 | 1–2 | 1 |
Valine | 3–7 | 2–7 | — | 3–5 | 2–6 | 5 | 3–7 | 5 | 6 | <1–5 | 5 | 10 |
Fatty acid (% of total FAME) | ||||||||||||
14:0 | — | — | 23 | <1–1 | 17 | 7 | 1–8 | 4–7 | — | 1–4 | 2–4 | 1–12 |
16:0 | 26–45 | 14 | 17 | 12–29 | 12 | 26 | 11–43 | 11–32 | 15–16 | 16–38 | 14–25 | 14–46 |
18:0 | 2 | 1 | <1 | 1–3 | 1 | — | 1–11 | 1–2 | 1 | 1–2 | 3 | <1–9 |
16:1n-7 | — | 2 | 28 | <1–1 | 3 | 38 | 2–31 | 19–43 | 2–3 | <1 | 1–26 | <1–13 |
17:1 | — | 4 | — | <1–5 | — | — | <1–10 | — | 4–5 | — | — | — |
18:1n-6 | 10–17 | — | — | — | — | — | — | — | — | — | — | — |
18:1n-9 | — | 45–47 | 1 | 5–44 | 7 | — | 1–12 | 3–9 | 24–30 | <1–27 | 4–7 | <1–43 |
18:1n-7 | — | 1 | 1 | — | 1 | — | — | <1 | — | <1 | 1–2 | <1–10 |
16:2n-6 | — | 3–4 | — | — | — | — | — | — | 2 | — | 1 | — |
16:2n-7 | — | — | — | — | 2 | — | — | 1–2 | — | — | — | — |
16:3n-4 | — | — | — | — | — | — | — | 1–4 | — | — | — | — |
16:4n-3 | — | <1 | — | — | — | — | — | — | 9–12 | — | 16–18 | — |
18:2n-6 | 11–12 | 21 | 1 | 20–33 | <1–4 | 3 | <1–19 | 1–6 | 13 | <1–2 | 4–7 | <1–10 |
18:3n-6 | 17–40 | — | 1 | 1–15 | <1–1 | — | <1–2 | — | — | <1 | — | <1–1 |
18:3n-3 | — | 6–7 | <1 | <1–40 | 1–6 | 1 | <1–32 | <1–3 | 18–23 | <1 | 5–22 | — |
18:4n-3 | — | 1 | <1 | 1–6 | 4–19 | — | <1–3 | <1–1 | 2–3 | <1 | 2–8 | <1–1 |
20:4n-6 | — | — | 6 | <1–7 | <1 | 4 | 1–6 | <1–1 | — | 1 | <1–4 | <1–15 |
20:5n-3 | — | — | 17 | <1–1 | <1–28 | 9 | <1–28 | 8–35 | — | 1–16 | 2–8 | 1–20 |
22:5n-6 | — | — | — | — | 2 | — | — | — | — | 1–7 | — | <1–21 |
22:6n-3 | — | — | 1 | — | 5–14 | — | <1–3 | <1–2 | — | 18–44 | <1 | 3–68 |
Mineral (%) | ||||||||||||
Calcium | 0.1–1.4 | <0.1–0.6 | — | — | 0.6 | — | 0.1 | 0.3 | 0.1–0.2 | — | 3.0 | — |
Magnesium | 0.2–0.3 | 0.1–0.8 | — | — | 1.0 | — | 0.3 | 0.7 | 0.1–0.2 | — | 0.4 | — |
Phosphorous | 0.1–1.3 | 0.3–1.8 | — | — | <0.1–2.6 | — | 0.7 | 1.2 | 0.5–0.7 | — | 1.5 | — |
Potassium | 0.6–2.6 | <0.1–2.1 | — | — | 1.2 | — | 1.5 | 2.4 | 0.6–0.7 | — | 1.9 | — |
Sodium | 0.4–2.2 | <0.1–1.3 | — | — | 1.6 | — | 1.0 | 2.7 | 0.1 | — | 0.9 | — |
Sulfur | — | — | — | — | — | — | 0.6 | 1.4 | — | — | 1.4 | — |
Trace element (mg kg−1) | ||||||||||||
Copper | 4 | 22–1900 | — | — | — | — | 18 | 55 | 15–25 | — | 102 | — |
Iron | 539–1800 | 198–6800 | — | — | 15 | — | 1395 | 4773 | 1081–1777 | — | 1774 | — |
Manganese | 19–37 | 20–4000 | — | — | 801 | — | 151 | 45 | 74–119 | — | 191 | — |
Selenium | 2 | 1 | — | — | — | — | <1 | <1 | <1–1 | — | <1 | — |
Zinc | 14–40 | 6–5500 | — | — | 19 | — | 32 | 50 | 38–63 | — | 64 | — |
Heavy metal (mg kg−1) | ||||||||||||
Arsenic | <0.1–2.9 | 0.1–0.5 | — | — | — | — | — | — | <0.1–2.4 | — | — | — |
Cadmium | <0.1–1.0 | <0.1–0.1 | — | — | — | — | — | — | <0.1–1.7 | — | — | — |
Mercury | <0.1–0.5 | <0.1–0.1 | — | — | — | — | — | — | <0.1–0.4 | — | — | — |
Lead | 0.1–5.1 | <0.1–2.0 | — | — | — | — | — | — | 0.6–6.0 | — | — | — |
3.3.2. Elemental composition
There are limited data on elemental composition of microalgae and this is in contrast to macroalgae (seaweeds) where numerous species have been well characterized. This is not overly surprising as it is well-documented that most microalgae (excluding some diatoms) typically contain far less inorganic (ash) content (generally <20%) than seaweeds (22–64%). Table 2 shows the mineral and trace element composition of microalgae genera that have been evaluated for salmonid feeds. With regard to the minerals most often required by farmed salmonids and therefore routinely supplemented in aquafeeds, calcium and magnesium levels in algal biomass are generally around 0.4% each while
3.3.3. Vitamin and carotenoid composition
Despite commercial claims of microalgae being vitamin-rich, there are minimal data in the literature on vitamin concentrations for a small number of species; namely
3.4. Nutritional evaluation of microalgae for use in salmonid feeds
When evaluating the nutritional quality of potential novel ingredients for aquaculture feeds, nutritionists take a logical step-wise approach which generally involves: (1) comprehensive characterization of their major biochemical components, trace elements, possible anti-nutritional factors (ANFs) and contaminants; (2) assessment of the palatability of diets containing these novel ingredients to estimate their potential effects on feed consumption/feed refusal; (3) estimations of their nutrient digestibility through
Genera | Form | Inclusion levels | Main findings | Ref. |
---|---|---|---|---|
Whole-cell meal | 0–9% | Can be included at 7% for rainbow trout without adverse effects on growth and body composition. | [11] | |
Whole-cell meal | 0–10% | Rainbow trout fed diets with 10% |
[12] | |
Whole-cell meal | 0–10% | Rainbow trout fed up to 10% |
[13] | |
Whole-cell meal | 0–30% | Digestibilities of |
[14] | |
Whole-cell meal | 100% | Protein digestibilities of 79–87% were estimated for |
[15] | |
Whole-cell meal | 0–50% | [16] |
Genera | Form | Inclusion levels | Main findings | Ref. |
---|---|---|---|---|
Whole-cell meal | 0–30% | Digestibilities of |
[14] | |
Whole-cell meal | 0–11% | [17] | ||
Whole-cell and cell-ruptured meals | 0–30% | EAA indices are high (0.9) for |
[7] | |
Cell-ruptured meal | 0–20% | 20% |
[18] | |
Lipid-extracted meal | 0–20% | Defatted |
[19] | |
Lipid-extracted meal | 0–30% | Digestibilities of |
[20] | |
Whole-cell meal | 0–5% | [21] | ||
Whole-cell meal | 0–24% | [22] | ||
Lipid-extracted meal | 0–30% | Digestibilities of |
[20] | |
Whole-cell meal | 0–24% | [22] | ||
Lipid-extracted meal | 0–17% | Defatted |
[23] | |
Whole-cell meal | 0–12% | [24] | ||
Whole-cell meal | 0–24% | [22] | ||
Whole-cell meal | 0–7% | [23] |
Genera | Form | Inclusion levels | Main findings | Ref. |
---|---|---|---|---|
Whole-cell meal | 0–9% | [25] | ||
Whole-cell meal | 0–20% | [26] | ||
Whole-cell meal | 0–5% | [27] | ||
Whole-cell meal | 0–20% | When included at 13% for Atlantic salmon, |
[26] | |
Whole-cell meal | 0–11% | [28] | ||
Whole-cell meal | 0–15% | [29] | ||
Whole-cell meal | 0–10% | [30] |
Genera | Form | Inclusion levels | Main findings | Ref. |
---|---|---|---|---|
Whole-cell meal | 0–10% | Inclusion of 7.5% |
[31] | |
Whole-cell meal | 0–10% | Inclusion of 10% |
[32] | |
Whole-cell meal | 0–64 mg Ax1/Cx2 blend kg diet−1 | Muscle pigment levels of rainbow trout fed |
[33] | |
Whole-cell meal | 0–64 mg Ax/Cx blend kg diet−1 | Inclusion of |
[34] | |
Cell-ruptured meal | 0–73 mg Ax kg diet−1 | All measured parameters were inferior when Ax was supplied by |
[35] | |
Cell-ruptured meal | 0–60 mg Ax kg diet−1 | [36] | ||
Whole-cell meal | 0–6% of diet (42 mg Ax / 44 mg Cx blend kg diet−1) | Muscle carotenoid retention of rainbow trout fed 6% |
[37] | |
Whole-cell meal | 0–1% | Inclusion of 0.3% |
[38] | |
Cell-ruptured meal | 0–74 mg Ax kg diet−1 | Scalable high-pressure processing of |
[39] | |
Cell-ruptured meal | 0–50 mg Ax kg diet−1 | Serum Ax levels were reduced in rainbow trout fed |
[40] | |
Extracted oil | 0–40 mg Ax kg diet−1 | Inclusion of Ax-rich oil extracts from |
[41] | |
Whole-cell meal | 0–30 mg Ax kg diet−1 | Inclusion of |
[42] | |
Whole-cell and cell-ruptured meals | 0–40 mg Ax kg diet−1 | Inclusion of |
[43] | |
Cell-ruptured meal | 0–80 mg Ax kg diet−1 | Weight gain of rainbow trout fed |
[44] |
3.4.1. Microalgae-based ingredients as protein sources
When evaluated as dietary protein sources for salmonid aquafeeds (Tables 3, 4), studies have been conducted using various freshwater and marine microalgae genera with rainbow trout (
3.4.2. Microalgae-based ingredients as lipid sources
The dietary essential n-3 LC-PUFAs, EPA and DHA, required by farmed salmonids have traditionally been supplied by fish oil, which is manufactured from wild-caught pelagic fish deemed unsuitable for direct human consumption, and this practice is no longer ecologically or economically sustainable. Historically, consumption of fatty fish like salmonids was the best means at achieving the recommended daily intake of 500–1000 mg of EPA and DHA for support of cardiovascular and neuronal health. However, partial or total replacement of fish oils in farmed salmonid feeds with terrestrial lipid sources has started to diminish the content of these essential n-3 LC-PUFAs. While rendered animal fats and vegetable oils commonly used in modern salmonid feeds provide excellent sources of digestible energy (calories) for farmed fish, they lack essential n-3 LC-PUFA that are responsible for dietary health benefits associated with fatty seafood consumption. Terrestrial based oils and fats in salmonid feeds has come at the expense of EPA and DHA levels in the end product for the consumer. As a result, there is tremendous interest and forward momentum for the partial or total replacement of conventional fish and plant oils and animal fats in salmonid feeds with high n-3 LC-PUFA products of microalgal origin. The most suitable candidates are predominantly strains of
3.4.3. Microalgae-based ingredients as carotenoid sources
In addition to microalgae as sources of essential nutrients, energy and LC-PUFAs, many also synthesize carotenoids and phycobiliproteins. Of particular interest is astaxanthin, which has become a rapidly growing area of study for the farmed salmonid aquafeed industry. The three predominant sources of commercially-available astaxanthin are chemical synthesis, yeast fermentation and algal induction. The cost of each are estimated at: synthetic (~$2,000 kg−1) <
4. Concluding perspectives
While microalgae-based products have tremendous potential as ‘next-generation’ feed ingredients for sustainable salmonid aquaculture, few have yet to successfully be commercialized and reach the marketplace. Strains of
Acknowledgments
The author greatly appreciates logistical support of Drs. Stephen O’Leary and Patrick McGinn and assistance of staff at the NRC-Marine Research Station. Thanks to Mr. Shane Patelakis and Drs. Stefanie Colombo and Stephen O’Leary for critical reviews of a draft of this manuscript and helpful suggestions to improve the quality of this chapter. Funding was provided by the National Research Council of Canada’s Algal Carbon Conversion program. This is NRCC publication no. 56379.
References
- 1.
Troell M, Naylor RL, Metian M, Beveridge M, Tyedmers PH, et al. Does aquaculture add resilience to the global food system? Proceedings of the National Academy of Sciences of the United States of America. 2014; 111 :13257-13263 - 2.
Gentry RR, Froehlich HE, Grimm D, Kareiva P, Parke M, et al. Mapping the global potential for marine aquaculture. Nature Ecology and Evolution. 2017; 1 :1317-1324 - 3.
Becker EW. Microalgae for aquaculture: Nutritional aspects. In: Richmond A, Hu Q, editors. Handbook of Microalgal Culture: Applied Phycology and Biotechnology. 2nd ed. United Kingdom: John Wiley and Sons, Ltd., Blackwell Publishing Ltd; 2013. pp. 671-691 - 4.
Görs M, Schumann R, Hepperle D, Karsten U. Quality analysis of commercial Chlorella products used as dietary supplement in human nutrition. Journal of Applied Phycology. 2010;22 :265-276 - 5.
Colombo SM, Wacker A, Parrish CC, Kainz MJ, Arts MT. A fundamental dichotomy in long-chain polyunsaturated fatty acid abundance between and within marine and terrestrial ecosystems. Environmental Reviews. 2017; 25 :163-174 - 6.
Sprague M, Betancor MB, Tocher DR. Microbial and genetically engineered oils as replacements for fish oil in aquaculture feeds. Biotechnology Letters. 2017; 39 :1599-1609 - 7.
Tibbetts SM, Mann J, Dumas A. Apparent digestibility of nutrients, energy, essential amino acids and fatty acids of juvenile Atlantic salmon ( Salmo salar L.) diets containing whole-cell or cell-rupturedChlorella vulgaris meals at five dietary inclusion levels. Aquaculture. 2017;481 :25-39 - 8.
Shah MR, Lutzu DA, Alam A, Sarker P, Chowdhury MAK, et al. Microalgae in aquafeeds for a sustainable aquaculture industry. Journal of Applied Phycology. 2017. DOI: 10.1007/s10811-017-1234-z - 9.
Matos AP. The impact of microalgae in food science and technology. Journal of the American Oil Chemists’ Society. 2017; 94 :1333-1350 - 10.
Engle C. The value of alternative feed ingredients. Journal of the World Aquaculture Society. 2017; 48 :377-380 - 11.
Ahmadzadenia Y, Nazeradl K, Ghaemmaghami Hezave S, Hejazi MA, Zamanzad Ghavidel S, et al. Effect of replacing fishmeal with Spirulina on carcass composition of rainbow trout. ARPN : Journal of Agricultural and Biological Science (JABS). 2011;6 :66-71 - 12.
Güroy D, Güroy B, Merrifield DL, Ergün A, Tekinay AA, et al. Effect of dietary Ulva andSpirulina on weight loss and body composition of rainbow trout,Oncorhynchus mykiss (Walbaum), during a starvation period. Animal Physiology and Animal Nutrition. 2011;95 :320-327 - 13.
Yeganeh S, Teimouri M, Amirkolaie AK. Dietary effects of Spirulina platensis on hematological and serum biochemical parameters of rainbow trout (Oncorhynchus mykiss ). Research in Veterinary Science. 2015;101 :84-88 - 14.
Burr GS, Barrows FT, Gaylord G, Wolters WR. Apparent digestibility of macro-nutrients and phosphorous in plant-derived ingredients for Atlantic salmon, Salmo salar and Arctic charr,Salvelinus alpinus . Aquaculture Nutrition. 2011;17 :570-577 - 15.
Tibbetts SM, Yasumaru F, Lemos D. In vitro prediction of digestible protein content of marine microalgae (Nannochloropsis granulata ) meals for Pacific white shrimp (Litopenaeus vannamei ) and rainbow trout (Oncorhynchus mykiss ). Algal Research. 2017;21 :76-80 - 16.
Dallaire V, Lessard P, Vandenberg G, de la Noüe J. Effect of algal incorporation on growth, survival and carcass composition of rainbow trout ( Oncorhynchus mykiss ) fry. Bioresource Technology. 2007;98 :1433-1439 - 17.
Burr GS, Wolters WR, Barrows FT, Hardy RW. Replacing fishmeal with blends of alternative proteins on growth performance of rainbow trout ( Oncorhynchus mykiss ), and early or late stage juvenile Atlantic salmon (Salmo salar ). Aquaculture. 2012;334/337 :110-116 - 18.
Grammes F, Reveco FE, Romarheim OH, Landsverk T, Mydland LT, et al. Candida utilis andChlorella vulgaris counteract intestinal inflammation in Atlantic salmon (Salmo salar L.). PLoS One. 2013;8 :e83213. DOI: 10.1371/journal.pone.0083213 - 19.
Kiron V, Sørensen M, Huntley M, Vasanth GK, Gong Y, et al. Defatted biomass of the microalga, Desmodesmus sp., can replace fishmeal in the feeds for Atlantic salmon. Frontiers in Marine Science. 2016;3 :67. DOI: 10.3389/fmars.2016.00067 - 20.
Gong Y, Guterres HADS, Huntley M, Sørensen M, Kiron V. Digestibility of the defatted microalgae Nannochloropsis sp. andDesmodesmus sp. when fed to Atlantic salmon,Salmo salar . Aquaculture Nutrition. 2018;24 :56-64 - 21.
Norambuena F, Hermon K, Skrzypczyk V, Emery JA, Sharon Y, et al. Algae in fish feed: Performances and fatty acid metabolism in juvenile Atlantic salmon. PLoS One. 2015; 10 :e0124042. DOI: 10.1371/journal.pone.0124042 - 22.
Skrede A, Mydland LT, Ahlstrøm Ø, Reitan KI, Gislerød HR, et al. Evaluation of microalgae as sources of digestible nutrients for monogastric animals. Journal of Animal and Feed Sciences. 2011; 20 :131-142 - 23.
Kiron V, Phromkunthong W, Huntley M, Archibald I, de Scheemaker G. Marine microalgae from biorefinery as a potential feed protein source for Atlantic salmon, common carp and whiteleg shrimp. Aquaculture Nutrition. 2012; 18 :521-531 - 24.
Sørensen M, Berge GM, Reitan KI, Ruyter B. Microalga Phaeodactylum tricornutum in feed for Atlantic salmon (Salmo salar ) - effect on nutrient digestibility, growth and utilization of feed. Aquaculture. 2016;460 :116-123 - 25.
Betiku OC, Barrows FT, Ross C, Sealey WM. The effect of total replacement of fish oil with DHA-gold® and plant oils on growth and fillet quality of rainbow trout ( Oncorhynchus mykiss ) fed a plant-based diet. Aquaculture Nutrition. 2016;22 :158-169 - 26.
Zhang C. Determination of the digestibility of a whole-cell DHA-rich algal product and its effect on the lipid composition of rainbow trout and Atlantic salmon. M.Sc. Thesis. Saskatoon: University of Saskatchewan; 2013. 87 p - 27.
Lyons PP, Turnbull JF, Dawson KA, Crumlish M. Effects of low-level dietary microalgae supplementation on the distal intestinal microbiome of farmed rainbow trout Oncorhynchus mykiss (Walbaum). Aquaculture Research. 2017;48 :2438-2452 - 28.
Sprague M, Walton J, Campbell PJ, Strachan F, Dick JR, et al. Replacement of fish oil with a DHA-rich algal meal derived from Schizochytrium sp. on the fatty acid and persistent organic pollutant levels in diets and flesh of Atlantic salmon (Salmo salar , L.) post-smolts. Food Chemistry. 2015;185 :413-421 - 29.
Kousoulaki K, Østbye TKK, Krasnov A, Torgersen JS, Mørkøre T, et al. Metabolism, health and fillet nutritional quality in Atlantic salmon ( Salmo salar ) fed diets containing n-3-rich microalgae. Journal of Nutritional Science. 2015;4 :e24 - 30.
Carter CG, Bransden MP, Lewis TE, Nichols PD. Potential of Thraustochytrids to partially replace fish oil in Atlantic salmon feeds. Marine Biotechnology. 2003; 5 :480-492 - 31.
Teimouri M, Amirkolaie AK, Yeganeh S. Effect of Spirulina platensis meal as a feed supplement on growth performance and pigmentation of rainbow trout (Oncorhynchus mykiss ). World Journal of Fish and Marine Sciences. 2013;5 :194-202 - 32.
Teimouri M, Amirkolaie AK, Yeganeh S. The effects of dietary supplement of Spirulina platensis on blood carotenoid concentration and fillet color stability in rainbow trout (Oncorhynchus mykiss ). Aquaculture. 2013;414/415 :224-228 - 33.
Gouveia L, Choubert G, Gomes E, Rema P, Empis J. Use of Chlorella vulgaris as a carotenoid source for rainbow trout: Effect of dietary lipid content on pigmentation, digestibility and retention in the muscle tissue. Aquaculture International. 1998;6 :269-279 - 34.
Gouveia L, Gomes E, Empis J. Use of Chlorella vulgaris in rainbow trout,Oncorhynchus mykiss , diets to enhance muscle pigmentation. Journal of Applied Aquaculture. 1997;7 :61-70 - 35.
Choubert G, Mendes-Pinto MM, Morais R. Pigmenting efficacy of astaxanthin fed to rainbow trout Oncorhynchus mykiss : Effect of dietary astaxanthin and lipid sources. Aquaculture. 2006;257 :429-436 - 36.
Moretti VM, Mentasti T, Bellagamba F, Luzzana U, Caprino F, et al. Determination of astaxanthin stereoisomers and color attributes in flesh of rainbow trout ( Oncorhynchus mykiss ) as a tool to distinguish the dietary pigmentation source. Food Additives and Contaminants. 2006;23 :1056-1063 - 37.
Choubert G, Heinrich O. Carotenoid pigments of the green alga Haematococcus pluvialis : Assay on rainbow trout,Oncorhynchus mykiss , pigmentation in comparison with synthetic astaxanthin and canthaxanthin. Aquaculture. 1993;112 :217-226 - 38.
Sheikhzadeh N, Tayefi-Nasrabadi H, Oushani AK, Enferadi MHN. Effects of Haematococcus pluvialis supplementation on antioxidant system and metabolism in rainbow trout (Oncorhynchus mykiss ). Fish Physiology and Biochemistry. 2012;38 :413-419 - 39.
Young AJ, Pritchard J, White D, Davies S. Processing of astaxanthin-rich Haematococcus cells for dietary inclusion and optimal pigmentation in rainbow trout,Oncorhynchus mykiss L. Aquaculture Nutrition. 2017;23 :1304-1311 - 40.
White DA, Page GI, Swaile J, Moody AJ, Davies SJ. Effect of esterification on the absorption of astaxanthin in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquaculture Research. 2002;33 :343-350 - 41.
Bowen J, Soutar C, Serwata RD, Lagocki S, White DA, et al. Utilization of (3 S ,3’S )-astaxanthin acyl esters in pigmentation of rainbow trout (Oncorhynchus mykiss ). Aquaculture Nutrition. 2002;8 :59-68 - 42.
Sheikhzadeh N, Panchah IK, Asadpour R, Tayefi-Nasrabadi H, Mahmoudi H. Effects of Haematococcus pluvialis in maternal diet on reproductive performance and egg quality in rainbow trout (Oncorhynchus mykiss ). Animal Reproduction Science. 2012;130 :119-123 - 43.
Sommer TR, Potts WT, Morrissy NM. Utilization of microalgal astaxanthin by rainbow trout ( Oncorhynchus mykiss ). Aquaculture. 1991;94 :79-88 - 44.
Sommer TR, D’Souza FML, Morrissy NM. Pigmentation of adult rainbow trout, Oncorhynchus mykiss , using the green algaHaematococcus pluvialis . Aquaculture. 1992;106 :63-74