Concerns are being raised about the negative consequences on world fishmeal production of overfishing. Fishmeal demand is likely to surpass the world’s supply by 2050. The continued aquaculture expansion is one of the main reasons for such increase in fishmeal demands (Halweil, 2008). Fish feeds are the highest recurring cost in fish farming. It comprises from 30 to 70 percent of the variable costs (Muzinic et al., 2006). Increasing fishmeal cost, irregular supply, decreasing availability, and poor quality of fishmeal have put forward highlighting on its partial or complete substitution with other alternative protein sources (Ramachandran and Ray, 2007). Currently, a lot of studies have been conducted to assess the partial or complete substitution of fishmeal in feed diets for tilapia with less expensive as well as locally available plant and animal protein sources (Fasakin et al., 2005; Borgeson et al., 2006; Gaber, 2006; Goda et al., 2007; Schuchardt et al., 2008; Soltan et al., 2008; Ali et al., 2008; Metwally and El-Gellal, 2009; Mohammad and Abdel-Tawwab, 2011; Labib et al., 2012; Abo-State et al., 2014; Hassan et al., 2015; Labib et al., 2015; Yones and Metwalli, 2015; Sharawya et al., 2016; Al-Asgah et al., 2016; Abdel-Warith et al., 2016). The review in hands aims to appraise the diverse types of fishmeal substituents and draw attention to the most proper alternatives in fish diets.

1 Materials and Methods

Data (in million metric tons) for the global and regional seafood supply have been extracted from recently published United Nations FAOSTAT reports (FAO, 2014; 2016). To explore the alternatives of fishmeal and the negative effects of climate change on fisheries particularly small pelagic fishes, the relevant peer-reviewed literature have been searched using Google Scholar and PubMed until January 2017. The following search terms: fishmeal, climate change, alternatives, protein sources, plant, and animal have been used. We also looked for relevant reports and articles and that were cited in other papers found through searching. The reports and articles used in this work cover animal feed, fish biology, environment, Nutrition, as well as aquaculture.

2 Results and Discussion

2.1 Status of global aquaculture production

Currently, fish plays a very important role in food security worldwide. It provides different types of nutrients, including protein, micronutrients, and omega-3 polyunsaturated fatty acids (Li and Hu, 2009). Aquaculture is the cheapest way to produce food rich in protein (Soliman and Yacout, 2016). Fish considered as the main source of protein from animals. It contributes to more than 25 percent of the total animal protein for about 1250 million people (FAO, 2009). With the relatively static production of captured fisheries since 1980, fish farming was in charge of the remarkable increase in the supply of fish for human consumption (Figure 2). While, fish farming supplied no more than 7 percent of the total human fish consumption in 1974, this share was grown to 26% in 1994 and 39% in 2004 (FAO, 2016). Fishery and aquaculture sectors are considered as a fundamental resource of income for millions of persons in low income families (Béné, 2006). In this respect it contributes directly as well as indirectly to their food security (Béné et al., 2007; Allison et al., 2011).

The exponential aquaculture growth sector during the past 2 decades is a result of the progressive production from intensive systems. A major contributor to this intensification is the use of manufactured feeds formulated to meet the increasing nutritional necessities of the targeted fish species (FAO, 2009). Intensive farming of carnivorous fish involves supply of additionally as well as nutritionally complete synthetically compounded aquafeeds. The accessibility and cost of such fishmeal and fish oil inputs is a nontrivial issue to fish farmers. Feed expenses showed to stand for up to 60 % of their total operation expenditure (Stickney, 1994).

2.2 Fishmeal in aquaculture

Fish is used as a direct human food. It contributes indirectly to human nutrition when it is utilized as fishmeal for poultry/livestock as well as aquaculture feeds (Tacon and Metian, 2009). Considerable, but decreasing, quantity of global fisheries production is processed into fish oil and fishmeal. This indirectly contributes to human consumption once it used as feed for fish and farm animals. Fishmeal is crude flour. It is acquired after milling and drying of fish or fish parts. On the other hand, Fish oil is apparent brown/yellow liquid. It is acquired after the pressing of the cooked fish. Fish meal and fish oil formed from a whole fish, fish by-products or fish remains. Many kinds of fish species are used for fish oil and fishmeal. Oily fish, particularly anchoveta is considered as the major kinds of utilized species. Also, anchoveta catches is affected by El Nino phenomenon. Stringent management procedures diminish catches of anchoveta and other species usually used for reduction. Therefore, fishmeal and fish oil production oscillates according to changes in the catches of these species (FAO, 2016). In 2011, 23 Mt of fish fundamentally from small pelagic fish species such as anchovy, mackerel, sardine, and herring destined to non-direct human consumption. 75% (17 Mt) of these fishes was reduced to fish oil and fishmeal for aquaculture, poultry and other farm animals feeding. In 2010, 73% of total world fishmeal was used to feed cultured fish, followed by pigs (20%), poultry (5%) and others (2%) (Shepherd and Jackson, 2013).

Fishmeal used for farmed fish and domestic animals raises important concern from a food nutrition and security perception. Leaving away the argue on the utilization of these small fishes in supporting larger fish, birds and marine mammals in the ecosystem (Smith et al., 2010), is fishmeal the most effective means to consume fish (particularly lower cost small pelagic fishes) or could these fish contribute more to the food security if a larger share of them was utilized directly via human consumption? In spite of some considerable progress in the last decade, the conversion rate of fishmeal to fish is still remains an issue of concern (Troell et al., 2014). On average, for every 1.0 kg of farmed fish produced, about 0.7 kg of wild fish is consumed (Tacon and Metian, 2009). This average figure, however, masks essential differences. The rate for omnivorous farmed fish, is dropped to relatively an acceptable level from 0.2 to 1.41 kg of wild fish per 1.0 kg of farmed fish. While, the figure is higher for carnivorous farmed fish: from 1.35 to 5.16 kg to produce 1.0 kg of farmed fish (Boyd et al., 2007).

The detailed fishmeal and fish oil production during 2004-2014 depicted in Figure 3. According to IFFO and Oil World data, the average yearly fishmeal production was projected at 5.238 million t. The maximum production (6.095 million t) registered in 2004. While, the minimum (4.136 million t) production registered in 2014. In 2006, there were some signs of a steep decline in the level of global fishmeal production (5.286 million t). It was estimated that the average annual production has been 4.9 million t until 2011, as compared with the average of 6.0 million t for 2001-2005. Thus, the average world fishmeal production in 2001-2005 was 6.0 million t compared to 4.9 million t registered in 2006-2010 with an El Nino occurring in 2003 and in 2010. Peru is the largest national producer which indicated that, in the absence of an El Nino, it represents about 25-30% of total global production. Chile came after Peru with around half of the Peruvian level. It is followed by Thailand. During the El Nino year of 2010, however, total global production dropped to only 4.1 million t and Peru’s share of world production dropped to only 19 percent. Whereas in 2010 global fishmeal production was the lowest since the early 1970s, the Peruvian fishery improved in 2011 and global production increased to about 5.2 (Shepherd and Jackson, 2009; Alicia, 2015). 2015 could see what is considered normal global supply levels of fishmeal at 5 million metric tons, and fish oil at 1m metric tonnes on March 5 at the tenth North Atlantic Seafood Forum (NASF) in Bergen, Norway. In 2014, fishmeal production was down 11.5 percent to 4.1 m over 2013 (Figure 3), while the fish oil output reached 843,000 t, down 7.5 percent year-on-year (Alicia, 2015).

The global share of fish production used for direct human consumption was significantly expanded during the latest decades. It is estimated at up to 67% in the 1960s to 87% or higher than 146 million tons in 2014. The left over 21 million tons was ordained for non human consumption products. Of which 76% was reduced to fishmeal and fish oil in 2014. The left over is used for a diversity of uses such as crude material for direct farmed fish feeding. The usage of byproducts is becoming an essential industry. There is an increasingly emergent center of attention on their usage in a safe, controlled, and hygienic way, thereby also reducing waste (FAO, 2016). Fish oil and fishmeal are the major digestible and nutritious inputs for cultured fish feeds. Fishmeal and fish oil required in feeds ingredients has shown a clear downward trend to offset their high prices, as feed demand increases, with their being more selectively utilized as strategic components at minor concentrations and for only definite stages of production, mainly hatchery, brood stock and finishing diets (FAO, 2016).

2.3 Climate change impacts on fishmeal production

Since 2005 production of fishmeal has declined gradually with the yearly oscillations affected by El Nino phenomenon. While, in general the production requirements have sustained to rise, pushing prices to unexpected historic highs during 2014. Prices then decreased until 2015 when high prospects for a strong El Nino started to push up prices again. Due to this continuous demand of fishmeal, higher prices are anticipated to remain in the long term. Total production was higher in 2015 compared to 2014, but Chile produced less. Peru and Chile, the main exporters, registered the lowest export volumes in the past six years in 2015. China remained the chief importer of fishmeal with 2015 import volumes equal to that in 2014 (FAO, 2016).

Aquaculture reliance on fish meal and fish oil becomes an important issue under most climate change scenarios (De Silva and Soto, 2009). Because capture fisheries are an important protein and lipids sources for aquaculture, changes in fisheries due to global climate change will impact aquaculture sector (Griffis and Howard, 2013).

In the North Atlantic, biological productivity is predicted to decrease by 50 percent while worldwide ocean productivity is predicted to being decreased by 20 percent due to climate change impacts (Schmittner, 2005). This would in turn greatly impact the availability of the small pelagic for fishmeal and oil production. The predicted changes in ocean circulation pattern might also have a negative influence on the reliability of small pelagic stocks that being utilized for fishmeal production. These changes in the fisheries productivity that cater to the fishmeal and fish oil industry, and particularly considered as the main fisheries on which production of fish oil and fishmeal is based, could limit the availability of raw materials (Griffis and Howard, 2013).

2.4 Potentials for fishmeal replacements in aquafeeds

Several studies on the different types of protein sources that have the ability of partially and/or totally replacing fishmeal in aquaculture feeds without affecting performance of growth rates of fish are being extensively studied (Tacon, 2004). Technology may lower the risks of higher prices and overfishing. It can provide substitutes to the use of captured fish derived inputs. Fishmeal and fish oil substitution in aquafeeds with nutritionally equivalent feedstuffs will diminish the reliance of different kinds of aquaculture on wild stocks. This substitution may also minimize pressure on prices of feed inputs that resulting from capture fisheries.

Recently, inclusion rates of fishmeal in aquaculture feeds have been declined. Promising results may be obtained by substituting protein rich oilseed and grain byproduct meals for fishmeal in carnivorous finfish and marine shrimp diets. These vegetable based substitutes comprise wheat gluten, soybean, rapeseed and corn gluten. Lupin and pea meals can be included. Other prospects for replacement may comprise terrestrial animal byproduct meals like meat and bone meal. On the other hand, these replacements may raise awareness about the perceived risks for the spread of different types of diseases (Delgado et al., 2003).

2.5 Plant by-products meals as alternatives protein source of fishmeal

The effectiveness of different types of alternatives protein sources as a partial or complete fishmeal substitution has been previously studied by many authors in fish diets, e.g. sunflower meal (Merida et al., 2011; Sultan et al., 2015), soyabean (Wu et al., 2016; Zhao et al., 2017; Wan et al., 2017; Yu et al., 2016), linseed meal (El-Saidy and Gaber, 2001; Soltan, 2005), canola (Slawski et al., 2013; Rajeev and Athithan, 2015), and cottonseed meal (Andreson et al., 2016; Ananyu et al., 2014), rapseed (Nagel et al., 2012; Slawski et al., 2012), pea meal (Collins et al., 2013; Fuertz et al., 2013; Gonzalez et al., 2016). However, the utilization of plant based proteins in aquafeeds resulted in a number of problems. These problems can be summarized as the occurrence of anti-nutritional factors, reduced digestability and issues of palatability (Hassan et al., 2015). Regardless of their typically high crude protein content, these fishmeal substituents are usually lacking in one or more essential amino acids. Theses limiting essential amino acids usually include lysine, isoleucine, and methionine (NRC, 1993). These imbalances can be overcome to a large extent by mixing complementary protein by-product meals so as to acquire the required essential amino acid profile (Davies et al., 1989).

Improvement of the nutritive value of these components by processing to increase the bioavailability of nutrients, diminish or remove anti-nutritional factors. On the other hand, the addition of proper additives could result in oilseed meals being incorporated at high levels in fish feeds (Wee, 1991). Furthermore, their shortage and competition from other sectors such as conventional crops for domestic animals and human consumption, as well as industrial use make their expenses is too high and put them far beyond the reach of fish farmers or producers of aquaculture feeds (Fasakin et al., 1999).

On the other hand, soybean has become an important source of biodiesel nowadays, thus, raising the world’s requirements for this crop, consequently, its prices. This results in the presence of anti-nutritional factors and nutritional profiles that do not fully match the fish requirements, especially with respect to amino acids and fatty acids (Geurden et al., 2005).

2.6 Terrestrial animal by-products

Terrestrial animal by-products have been extensively used as protein sources for tilapia. It includes blood meal, poultry by-product meal, hydrolyzed feather meal and meat and bone meal. It has high protein content in addition to good essential amino acid profiles (Tacon, 1993). Previous studies concluded that animal protein components can be valuable for fish feed formulation. They are rather much less expensive than fish meal (Hernandez et al., 2014; Sierra et al., 2014; Kritsanapuntu and Chaitanawisuti, 2015; Yu et al., 2015; Yones and Metwalli, 2015).

Poultry by-product meal is limited most in lysine (Nengas et al., 1999), while methionine was reported as the most limiting amino acid in meat and bone meal and blood meal. Furthermore, hydrolyzed feather meal is limiting in both lysine and methionine, while blood meal is also deficient in iso-leucine. However, some suggested way of overcoming these deficiencies is by supplementing the deficient amino acids or by mixing complementary alternatives to obtain the desired essential amino acid profile.

2.7 Fishery by-products

The likelihood of substituting fishmeal with fishery byproducts, such as shrimp head meal, fermented fish silage, squid meal, tuna by-product powder, tuna liver meal, fermented skipjack tuna viscera, and tuna head hydrolyzates have been tested in various aquaculture feeds (Uyan et al., 2006; Gumus et al., 2009; Iranshahi and Kiaalvandi, 2011; Nguyen et al., 2012; Hernandez et al., 2013; Lee et al., 2014).

2.8 Novel proteins

Finally, novel proteins is another area of active research in the aquaculture feed industry. Novel proteins are proteins obtained from single cell organisms and invertebrates, but they are often too costly to be considered as an alternative protein source to fishmeal in aquaculture feed. However, because of the recent increasing cost of fishmeal, researchers have started evaluating the economic feasibility and optimum usage of these novel proteins as fishmeal substitutes. Partial fishmeal replacement with algae is also possible (Kiron et al., 2012; Al-Asgah et al., 2016; Abdel-Warith et al., 2016; Radhakrishnan et al., 2016; Kiron et al., 2016; Kissinger et al., 2016), especially in tropical areas where they are found in plentiful amounts. Kiron et al. (2016) observed that partial substitution of fishmeal with defatted biomassof Desmodesmus sp. in the feed of Atlantic Salmon does not have any adverse effects on the specific growth rate, condition factor, protein efficiency ratio and whole body proximate composition of fish. Furthermore, the algal inclusion did not impair the health of Atlantic salmon. It is evident from the physiological indexes, molecular markers of inflammation and intestinal micromorphology.

2.9 Economic evaluation of fishmeal alternatives

Although some of the protein sources explained earlier probably leads to considerable decrease in fish performance, they still may be more cost effective than standard, costly proteins fishmeal. However, only a comparatively few studies have been measured both economic and biological estimation of dietary protein sources. These studies noticed that different sources such as cottonseed meal (El-Sayed, 1990), corn gluten feed and meal (Wu et al., 1995) animal by-product meal (Rodriguez-Serna et al., 1996; El-Sayed, 1998) and brewery waste (Oduro-Boateng and Bart-Plange, 1988) may be used as total fishmeal substitutes for tilapia even though they produced relatively minor biological performance. So, in order to get additional econonomically sustainable, environmentally friendly, and feasible production, research interests has been going towards the estimate and make use of unconventionally protein sources (Oduro-Boateng and Bart-Plange, 1988; Abo-State, 2014). Certainly, more research work in required in conjunction with this line.

3 Conclusion

Aquaculture is a significant player in human nutrition and global food supply, especially for poor people. Intensification of aquaculture production has made its demand for fishmeal from small pelagic fishes as an increasingly socioeconomically and environmentally important issue. Therefore, partial or complete substitution of fishmeal with less costly, locally accessible protein sources may be inevitable. By reviewing the current status of global aquaculture, fishmeal production and its contribution in fish feeds, and the different types of fishmeal alternatives, it was found that the inclusion of fishmeal alternatives in aquafeeds represents a number of problems which take account of the occurrence of anti-nutritional factors, reduced digestability, issues of palatability, reduction in fish growth an performance and resource use conflicts. On the other hand, still they could be more cost/effective than standard, expensive proteins; fishmeal. Researchers should start to evaluate the economic feasibility and optimum usage of novel proteins as fishmeal substitutes. Furthermore, improvement of local raw materials to be used in fish feed formulation is also highly recommended.

It is concluded that the idea of managing dynamic ecosystems throughout elastic, adaptive, ecosystem based management systems is getting enormous support (Garcia and Cochrane, 2005). Sustainability of natural resources and ecosystem services rely on how community can responds to ecosystem alterations resulted from mutual climatic and utilization patterns, rather than on their individual effects per se. In this respect, finding different types of novel sustainable protein sources has grown to be a major drive in the aquaculture industry consecutively to decrease dependence on fishmeal as the foremost protein component in aqua feeds (Hardy, 2010).

Authors' contributions

Naglaa F. Soliman and Mahmoud A. Hassaan participated in the sequence alignment and drafted the manuscript. Dalia M. M. Yacout participated in the final version of manuscript and data collection. All authors read and approved the final manuscript.

Acknowledgments

This research work is part of a research project sponsored by the IDRC Canada for establishing Alexandria Research Centre for Adaptation to Climate Change (ARCA).

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