Issues in Salmon Aquaculture Industry

### **Chapter 4**

## Perspectives on Salmon Aquaculture: Current Status, Challenges and Genetic Improvement for Future Growth

*James E. Barasa, Purity Nasimiyu Mukhongo and Cynthia Chepkemoi Ngetich*

#### **Abstract**

With an estimated global value of US\$15.6 billion, farmed salmonids represent a precious food resource, which is also the fastest increasing food producing industry with annual growth of 7% in production. A total average of 3,594,000 metric tonnes was produced in 2020, behind Chinese and Indian carps, tilapias and catfishes. Lead producers of farmed salmonids are Norway, Chile, Faroe, Canada and Scotland, stimulated by increasing global demand and market. However, over the last 2 years, production has been declining, occasioned by effects of diseases as well as rising feed costs. Over the last year, production has declined sharply due to effects of covid-19. This chapter reviews the species in culture, systems of culture, environmental footprints of salmon culture, and market trends in salmon culture. Burden of diseases, especially Infectious pancreatic Necrosis, Infectious salmon anemia and furunculosis, as well as high cost of feed formulation, key challenges curtailing growth of the salmon production industry, are discussed. A review is made of the international salmon genome sequencing effort, selective breeding for disease resistance, and the use of genomics to mitigate challenges of diseases that stifle higher production of salmonids globally.

**Keywords:** salmon, smolts, salmon genome, fish meal, parr, anadromous

#### **1. Introduction**

Salmonids constitute a large group of teleost fishes thriving in the cold-water fisheries and aquaculture. Salmonids belong to the family Salmonidae, comprising 11 genera, including the salmon, trout, charr, ciscos, grayling, hucho and the freshwater whitefish [1]. The sub-family Salmoninae groups three well known genera: *Onchorynchus*: rainbow trout, cutthroat trout, Pacific salmon, all with native ranges in the North Pacific Ocean. The genus *Salmo* groups the Atlantic salmon, Atlantic trout and the brown trout, all with native ranges in the North Atlantic Ocean. *Salvelinus* comprises the charr, with native ranges in the Pacific shores. The Pacific salmon has 5 species: chinook (*Onchorynchus tshawytsha*), chum (*O. keta*), coho (*O. kisutch*),

casu (*O. masu*), pink (*O. gorbuscha*) and sockeye (*O. nerka*) [2]. Pacific salmon are basically anadromous (migrate to sea water after spending early life in streams and rivers), semelparous (reproduce only once in a life time) and exhibit accurate homing. Atlantic salmon which inhabits the eastern coast of North America, are homing and iteroparous (reproduce more than once in a life time) [3].

Salmonids are the third largest farmed fin fish crop, behind Chinese and Indian carps and tilapias, with a total annual production of 3,594,000 metric tonnes [4]. They however form the lead farmed carnivorous fin fish globally. Production of salmon (Atlantic and Pacific salmon) forms the fastest growing food producing industry in the world, with annual growth of 7%. Atlantic salmon, *Salmo salar*, is iconic, high value, widely traded global fish product, and natural stocks are often threatened by overexploitation and habitat degradation [5]. It contributes substantially to food, economic and employment security in many countries, especially Norway, Chile, Canada and the United Kingdom [5], which are lead producers of the species (**Table 1** and **Figure 1**).

Significant development in the farming of *S. salar* is recorded in temperate coastal regions of countries such as Norway, Canada and Scotland [6], with Chile being among the top producers. A total of 30,000 direct and over 14,500 indirect jobs are provided by the salmon industry in Chile [7], underscoring the importance of salmon industry in the country, which is also the second biggest producer of farmed salmonids globally, with annual production averages of 700,000 tonnes [8]. Farmed salmonids account for over 73% of aquaculture production in Chile and became the second largest contributor to the Chilean economy [9], with the three most intensively farmed salmon species being *S. salar*, *O. mykiss* and *O. kisutch* [10]. In Scotland, salmon farming takes place on the west coast and islands of Scotland and approximately 95% of the aquaculture industry is dominated by *S. salar*, making it the third largest producer after Chile and Norway [7]. These countries are located within certain southern hemispheres that are at a constant temperature of around 0–20°C. Salmon farming ideally requires temperature of 13°C [11], or below. But the fish's appetite for food reduces at very low temperatures, and can therefore affect growth rates. Typically, juvenile fish less than 250 g (raised in freshwater) are released in to pens or cages in the ocean, where they are grown to market size of 2–8 kg a piece, within a grow-out period of 16–24 months. Before reaching 250 g for release to pens or cages, the early forms grow in wide areas of freshwater farms and hatcheries across eastern and southern Chile [12]. Thereafter, they are released for fattening in the marine environments in the southern most Patagonian fjords [13]. These areas are endowed with ample water flow in current, protected naturally by fjords and archipelagos.

With average growth in annual production of about 9%, salmonids represent the fastest growing food production system globally over the years, highlighting the important role of the fish in food and nutrition security, as well as livelihood and income generation. Salmon is rich in protein, omega-3 fatty acids, minerals and vitamins. In this respect, the Atlantic salmon is iconic in value, distribution and conservation status. With an increasing demand globally, consumption of salmon is currently 3 times its quantity for 1980, and contributes 70% of the market for salmonids. Apart from its high global demand, the high visibility of salmon on the market is due to the high level of industrialization and low-level risk associated with its culture. Contrary to its status of a luxury commodity in the 1980s, it is a major food item in the USA, Europe and Japan, with high prices of about US\$11.9 in USA and US\$ 7.3 per kg in Europe. High demand is also driven by lucrative emerging markets in China, Russia, and Brazil [14]. Farming *S. salar* is also much more efficient, about 8 times more efficient than beef production.

#### *Perspectives on Salmon Aquaculture: Current Status, Challenges and Genetic Improvement… DOI: http://dx.doi.org/10.5772/intechopen.101531*


**Table 1.** *Global production of lead farmed fish species 2017–2020 (000 metric tonnes).*

#### **Figure 1.**

*Global production of farmed* Salmo salar *(1998–2021), in metric tonnes. A steady increase in production is recorded annually over the years, demonstrating the importance of the species as food and source of income in main global producing countries.*

#### **1.1 Anadromy in Atlantic salmon**

Most salmonid species are anadromous. Hence, they spawn in freshwaters (streams, lakes and rivers), where the young ones spend 1–3 years before juvenile stages migrate to the sea for feeding and fattening. The ability to switch lifestyle from freshwater to sea water is called smoltification, a process controlled by temperature and photoperiod. As the fish mature in the sea, they begin to return to their point of release or spawn, in a process called homing, for spawning. Most salmons are semelparous, i.e. they breed only once in their life time and then die. Death is mainly due to exhaustion from the long distances covered during homing, and the excessive energy spent during spawning. A few salmons are iteroparous, i.e. spawn severally in their lifetime. This is because they are able to migrate back to the sea, after spawning to continue feeding and rebuilding their reproductive capacity. However, some species, such as rainbow trout complete their life cycles in freshwater. Anadromous salmon shows fidelity to the freshwater site at which they were spawned, or released, and therefore when they reach sexual maturity and are about to start breeding, they migrate back to these sites for spawning. The return of mature salmon to their natal streams from the ocean is called homing, a complex process in which majority of the fish return to their actual natal streams, while a few veer off to different streams.

#### *Perspectives on Salmon Aquaculture: Current Status, Challenges and Genetic Improvement… DOI: http://dx.doi.org/10.5772/intechopen.101531*

Suitable environmental conditions for growth of salmon include: low water temperatures of 8–16°C, clean and well aerated waters and well protected fjords, free from storms and other environmental upheavals [14]. These low temperatures reduce stress to the fish during summer, and reduce the growth rate in winter, conditions suitable for minimizing disease incidences among salmonids. Typically, these conditions are found in Norway, Chile, the North Atlantic and North Pacific coasts, as well as coastlines of Tasmania and New Zealand. These are countries of higher latitudinal ranges, often temperate regions. Although it is generally regarded that fish production increases with reducing latitudes, especially for warm water species [15], production of cold-water species nevertheless positively increases with increasing latitudes [15]. Although for warm water species, the effect of temperature on fish production in a fishery is generally boosted by the fertility of the waters [16], temperature is probably the main factor driving productivity of salmonids [15], given that most salmonid species are generally farmed in sea ranches or raceways on fish farms, systems that require clean, well aerated waters.

As high value species of global demand in the developed countries, salmonids are usually cultured in intensive systems, characterized by high fish densities, low water flow, and high concentrations of dissolved oxygen. Removal of carbon dioxide, solids and excretion end-products, such as ammonia and nitrites, are generally prioritized, in order to improve growth and health of the fish. Generally, *S. salar* has a low tolerance to a dissolved oxygen deficit, sensitive to increased concentrations of carbon dioxide, un-ionized ammonia and nitrites in freshwater.

#### **2. Main aquaculture systems used in salmon production**

#### **2.1 Flow through systems (FTS)**

Flow through systems, also called raceways or semi-closed culture systems, are culture units in which water flows continuously, making a single pass through the unit before being discharged. Raceways are mainly concrete, but some are earthen, lined with waterproof materials, yet some are fabricated from wood, fiber glass, metal, plastic and other materials, depending on the resources of the farmer. They are majorly designed for highly intensive culture and especially suitable for fish species that need constantly flowing clean water e.g. juvenile salmon and in the production of smolts. As high value species therefore, almost 80% of *S. salar* smolts globally are produced in flow through systems before being stocked in sea cages. Egg-larvae (parr) are supplied with fresh water from local sources such as rivers, lakes, ground water or natural springs at hatcheries and fish farms. Good flow rates and velocity of water is essential to the health of the stock under culture, and to flush wastes from the system. Water quality is maintained by treatment and manipulation of the flow rate of the water. The quality is then enhanced by injection of oxygen using air blowers, in order to minimize the water flow rate to 0.6 L/kg/min. Sophisticated farms heat the water to a certain temperature and manipulate light intensity [6]. Appropriate stocking density of the fish in FTS is dependent on water quality, management skills and general husbandry practices put in place, as well as the biology of the species, including the ability of the fish to tolerate crowding. FTS are capable of supporting a high number of smolts yearly, with averages of 900 million smolts in Norway alone produced under FTS [17]. Fish reared in these systems can however be highly susceptible to diseases due to stress caused by overcrowding. Raceway systems can be earthen or concrete based, majority are constructed from concrete or cement blocks.

#### **2.2 Recirculation system (RAS)**

Recirculation system was developed in the 1970s, to reduce the required amount of water and resultant waste produced from traditional flow through system. The system is highly controlled, and therefore requires substantial skills and input. In order to reduce the demand for large amounts of water, the system involves recirculation of water, which also reduces water wastage. Since water is recirculated in the system, there is enhanced biosecurity on salmon fish farms and hatcheries, and this prevents or minimizes escapee fish to the natural environment. Prevention of escapees from farms or hatcheries comes with several benefits, such as preservation of the purity of local natural populations of salmon, reduced incidences of disease and parasites to the natural populations, as well as to those within farms [18]. Wastes from fish are controlled and easily collected, which reduces pollution of the environment and the collected waste is easily aggregated for subsequent use for other purposes on the farm. Additionally, the environment for fish growth is optimized, with control of water temperature, water quality, feeds, and these maximize growth rates of the fish. Due to its ability to minimize impacts to the environment, RAS is easily and locally sited to markets, which therefore reduces transportation costs and carbon footprints, while simultaneously improving traceability and freshness of the product, and profitability of the enterprise as well.

Improved RAS systems comprise of two portions, with one part of the tank dedicated to fish rearing and trapping of particles and draining of sludge [19]. The other part is the water treatment system, composed of an additional solid removal system, submerged biofilter and an airlift for water circulation and gas exchange [19]. This therefore allows addition of oxygen and removal of carbon dioxide and ammonia gases from the water. Additional mechanical filters aid the removal of particles that would not settle. Generally, the efficiency of the RAS is enhanced, in order to reduce the amount of energy required to produce a kg of fish, while maximizing the stocking density of the fish (typically 61–122 kg/m3 , but in some cases, may exceed 545 kg/m3 ). The system is therefore successfully applied to rear smolts in many salmon producing countries [20]. In Norway, a total of 12–20 million smolt per year are produced under RAS [21]. Averagely, 350,000 MT of salmon are produced annually under RAS [22]. High technological complexities that necessitate high costs of production and highly skilled and competent human resource is the key challenge facing salmon farmers that operate RAS.

#### **2.3 Cage culture**

Cages or pens are natural or semi-sheltered bay where the shoreline forms all but one side of the enclosure. Cages or pens are made from bamboo, wooden poles or stakes driven into the substrate, the mesh size is typically small enough to retain the cultured fish but large enough to allow entry and exit of small fish and food organisms. Its management is less complex than land-based systems, make use of existing water bodies which gives local non-land owners access to fish farming. This type of system makes the majority of the salmon grow out particularly for seawater operations, and is appealing to most farmers, for incurring the lowest production and operation costs of all the production systems.

Cages are movable and float off the bottom, range from about 1 m<sup>2</sup> to over 1000 m<sup>2</sup> in surface area, with a depth of about 20–50 m, and a maximum circumference of 157 m. The stocking density limits for post smolt *S. salar* in commercial scale culture averages 75 kg/m3 [23]. Average production volumes almost doubled in Norway, increasing from 37 to 67 million m3 from the year 2005–2009, mainly due to better quality of water, better food organisms and reduced impact of storms. *Perspectives on Salmon Aquaculture: Current Status, Challenges and Genetic Improvement… DOI: http://dx.doi.org/10.5772/intechopen.101531*

Escaped fish, predation by seals and climate change are the main challenges facing cage culture of salmon.

#### **3. Marketing of salmon**

As an iconic group of fishes, salmon is very rich in high quality proteins, and long chain omega-3 fatty acids, which reduce the risk of cardiovascular disease and other health issues. It is a good source of minerals (iodine and selenium), vitamins (D and B12) and macronutrients. Due to this important nutritional composition, salmon is a globally traded product, especially in the developed countries, where purchasing power is also high.

#### **3.1 Processing of salmon**

In order to increase safety of the product, preserve high quality characteristics, extend shelf life and enhance economic returns to the producer, salmon is processed in different forms [24]. About 47% of the EU market supply of salmon is filleted, while 12% is of whole fish form, which is also the most preferred since they are fresh and preserved through chilling and freezing. A total of 28% of the supply is smoked salmon, while 13% constitute other value-added products [25]. Smoked salmon is the most expensive, sold at €90 a kilo, while fillets cost €14 a kilo [25]. Processing plants are required to ensure that the weight, color, size, shape and packaging of the final product are of the standard desired by the final consumer. This requires well trained and skilled workers to assure product quality. In this regard, and in an effort to maintain the highest standards of safety and hygiene of this globally traded fish product, processing facilities are often certified by US and EU authorities for them to qualify to supply export markets (**Figure 2**). Some of the requirements for this certification is the maintenance of solid cold chains, international standards of germ

#### **Figure 2.**

*Percentage of salmon producing companies in each of the main global salmon producing countries that are certified by Aquaculture Stewardship Council (ASC). Some of the criteria used by the ASC for certification of production value chain includes: the amount of fish meal used in formulating fish feed and fish oil for the farmed salmon, the amount of chemicals and drugs used in control of parasites and diseases, and biosecurity or the level of control put in place on fish farms to limit escape of farmed fish to the natural environment, lethal incidents involving marine mammals, antibiotic use and viral disease mortality. Fish from certified farms should be more attractive to export markets.*

control, i.e. the Hazard Analysis of Critical Control Points (HACCP) certification and efficient systems of waste management. As happens with other fish products, salmon processors also undertake value addition, to increase the shelf-life and value as well as expand the market [26]. The main value-added products of salmon include fillets, salmon bread, sushi, and smoked salmon [26]. Apart from improved purchasing power and awareness of nutritional benefits of consumption of salmon, this hygienic standards in processing the product and value addition have seen increased consumption of the product (**Figure 3**). A total consumption of farmed Atlantic salmon of 2.4 million tonnes was estimated in 2020 [4], which, when combined with those from capture fisheries rises to 3.2 million tonnes.

#### **3.2 Packaging of salmon**

Packaging is crucial for providing useful information to the consumer, such as product identity, origin, how to use and store, nutritional information among others. Well packaged fish products enhance efficient mechanized handling, distribution and marketing. Rigid materials like cans, glass container jars, plastic bags, pouches, film, sheets, jars and boxes are commonly used in packing salmon [27]. Fresh fish are usually loaded in plastic boxes that are hygienic, light and strong. The boxes are insulated to maintain the temperature of iced fish, while also allowing drainage of any melted liquid from the fish [27]. Frozen fish is commonly packed in interlocking, printed, polycoated and corrugated fiberboard cartons and expanded polystyrene and corrugated polypropylene boxes, sealed with polypropylene or metal tape. This type of boxes are also used for freezing wet fish, storing wrapped or unwrapped frozen fish [27]. Fresh, chilled or frozen fish are packed using Styrofoam, polyvinylidene chloride or polystyrene trays wrapped with cling film made from either polythene or polypropylene. Although this type of packaging can

#### **Figure 3.**

*Total imports of salmon by major consuming countries or regions from 2015 to 2020. USA is the United States of America, EU-UK is the European Union and the United Kingdom.*

*Perspectives on Salmon Aquaculture: Current Status, Challenges and Genetic Improvement… DOI: http://dx.doi.org/10.5772/intechopen.101531*

be attractive to customers, they cannot protect the fish from mechanical damage, loss of moisture and aroma or even contamination from microorganisms and odor from other products [27].

#### **3.3 Freight packaging**

Fresh, frozen or live salmon for airfreight is packaged in containers made from metal, fiberglass and expanded polystyrene. Such a container is insulated, easy to handle, heavy to give physical protection to the products and watertight to protect against contamination [27].

The main importing countries or regions for salmon products include the USA, EU-UK, Russia, Brazil and Asia. Although imports or consumption of salmon has been decreasing in the EU-UK, Russia and Brazil since 2016, consumption of salmon products has been on the increase in the USA and Asia (**Figure 3**), causing an increase in imports. The decline in Russian imports is occasioned by an embargo on salmon imports from Norway following the EU's trade sanctions against Russia due to the conflict in Ukrain.

#### **4. Main challenges in salmon aquaculture**

#### **4.1 Incidences of diseases**

The main diseases in farmed salmons include infectious salmon anemia (ISA), characterized by pale gills and fish that swim close to the water surface while gulping for air. Some cases are asymptomatic, but the fish die suddenly. ISA was first reported in Norwegian salmon farms in 1984, from where it spread to other big producers of salmon, causing huge losses of up to €100 million [28, 29]. ISA is caused by a virus, the Infectious salmon anemia virus, one of the most devastating diseases of marine farmed *S. salar*, and mainly attacks the grow out stages of the fish. In Chile, the first outbreak was in June 2007, with the ISAV HPR7b variant in circulation [30]. The impact of the outbreak was devastating, and was partly responsible for the brief decline in global production of salmon in subsequent years (**Figure 4**). ISA outbreaks come with high mortality of fish, huge loses to farmers and severe restriction to production in surrounding areas. A large number of risk factors are known to predispose salmon to ISA outbreaks [32]. Presence of the ISAV receptors in the fish, the variant strain (whether virulent or non-virulent) responsible for an outbreak, rate of evolution of the strain from non-virulent to virulent, the rate of viral reproduction and shedding, suboptimal management practices at cage farms, fish stocking and fallowing routines in cages, related disease outbreak events, level of intensification in fish production on the farm, and handling and treatment of fish constitute some risk factors that fuel increased incidences of ISA outbreaks [33–35]. Increased biosecurity, advanced fish husbandry practices, as well as a better understanding of some of the risk factors constitute suitable mitigation measures for ISA outbreaks [32].

Infectious pancreatic necrosis (IPN) is a disease of young salmonids (*Salmo*, *Onchorynchus* and *Salvelinus*), attacking the pancreas and liver parenchyma of the fish. The virus responsible for IPN is an *Aquabinarvirus* of family Birnaviridae, and comprises a bi-segmented double stranded RNA. Severe necrosis of pancreatic and liver cells occurs, which extends to the intestinal mucosae [36]. Post-smolts darken in color, anterior part of the abdomen swells, capillaries around the pectoral fins engorge, the dorsal fin erodes, while the vent swells [36]. It occurs both in freshwater and marine water stages, when the fish is typically of start-feeding stage to about 20 g (after

**Figure 4.**

*Production of Atlantic salmon (*Salmo salar*) in the 5 largest producer countries from 1992 to 2018. Norway remains the lead producer, followed by Chile over the years. Adopted from Iversen et al. [31].*

transfer to the seas in post-smoltification stage). Therefore, the disease attacks fry and post-smolts, and becomes especially severe in the marine environments (post-smolts), causing substantial mortality [37]. Effects of IPNV outbreaks are therefore economic, ecological, and social (welfare), since the salmon that survive the attack often remain asymptomatic carriers of the virus [38]. Economic losses due to IPNV outbreaks in Norway, for instance were estimated at US\$ 30 million [39]. Apart from presence in the pancreatic cells, some of the virus cells hide and therefore multiply and persist in the leucocytes of the head kidney. This leads to recurrent outbreaks, which spread quickly across farms in a locality, especially in lead salmon producers like Norway, and Chile where farms are concentrated in a locality. Some of the host defense mechanisms against IPNV include the interferon necrosis (IFN) factor and the anti-viral protein or gene Mx [40], which suppress the persisting viral cells. Following the introduction of IPN resistant strain (IPN-QTL) homozygous in salmon producing countries, mortality now varies based on the susceptible and resistant strains of salmon during the outbreak. Therefore, mortality can vary from 5 to 10% in the resistant strains of salmon, to 70% in the genetically susceptible strains in sea cages. This suggests that considerable gains against diseases in farmed salmon production can be made by a combination of selective breeding of salmon for disease resistance and a suite of both natural and active immune responses against invading pathogens.

Apart from infecting salmonids, furunculosis is also highly pathogenic for other fish species of the wild waters as well as farmed populations. It is caused by a gram-negative rod bacterium, *Aeromonas salmonicida* subsp. *salmonicida*. The bacterium carries an external surface layer, the A-protein surface layer (A-layer), which counters the host defense mechanisms of the fish. This is boosted by a lipopolysaccharide, a protective cell envelope antigen on the surface of the bacterium [41]. As the bacteria grow, they release extracellular products, which cause lesions *Perspectives on Salmon Aquaculture: Current Status, Challenges and Genetic Improvement… DOI: http://dx.doi.org/10.5772/intechopen.101531*

on the fish. Therefore, symptomatic cases are characterized by fish with lesions that lead to mortality in severe cases [41]. Infected fish are generally lethargic, lack appetite, develop dark skins, show ventral haemorhage at the base of anal, pectoral and pelvic fins, splenomegaly and subcapsular haemorhage occur in the liver [41]. When liquefactive skin lesions and ulcers rupture, more bacteria are released in to the environment, and increase infection of the surrounding fish. Severe outbreaks are reported to cause economic losses in excess of US\$100 million in Norway salmon Industry [28]. Control measures during outbreaks include prophylaxis, such as use of vaccines. Drugs (antibiotics such as flumequina) against furunculosis may be administered to the infected fish through diets, while best management practices are recommended to avoid outbreaks. In case of severe outbreaks, movement of smolts may be banned (quarantining farms), and farms that suffer outbreaks are banned from sale of smolts [41]. Common risk factors that induce outbreaks of furunculosis in salmon farms include: migration of fish, water quality, sharing or transfer of staff among salmon farms and hatcheries, breach of quarantine protocols and poor husbandry and hygienic practices of hatcheries and farms [42]. Additionally, algal blooms, increasing temperatures and salinity in wild waters increase the risk of outbreak of furunculosis [43].

#### **4.2 High cost of feeds for salmon production**

As a carnivorous fish group, farmed salmonids require high quality feeds (high crude protein content) for fast growth, and to attain appropriate nutritional composition. Typically, feeds for salmon comprise of: 93.4% dry matter, 35.6% crude protein, 33.5% crude lipid, 11.0% carbohydrates and 1.3% phosphorus [44]. However, formulating and maintaining such high-quality diets is not only expensive, but also environmentally challenging, as it requires high amounts of marine fish resources to provide the ingredients for protein and oils, which invariably increases overexploitation of resources (overfishing). In this regard, formulation of suitable diets for farmed salmon requires inclusion of fish meal and fish oil in appropriate quantities, to give the final product the required nutritional quality and composition. Usually, formulated diets for salmon constitute 40–60% fish meal and 20–30% fish oil, sourced mainly from marine anchovies, mackerel, pilchards, herring and blue whiting [45]. These marine fish species are often targeted as sources of fish meal and fish oil for salmon feed production because they provide appropriate nutrients for carnivorous fish species and offer appropriate amounts of polyunsaturated fatty acids (omega 3), in the fillets of the salmon, which is beneficial for human health. Notwithstanding the benefits of using fish meal and oils in salmon diet for human health, the practice not only makes salmon diets expensive, but also increases overfishing of target marine fish species, and so runs contrary to sound principles of conservation of aquatic biodiversity. Since the mid-2000s, the prices of fish meal and fish oil rose between 50 and 130% [46]. Such increases in the costs of key ingredients, coupled with the fact that traditionally, fish feeds form the highest cost of total fish culture enterprises, feeds for farmed salmon production provide a critical challenge in the global culture of salmonids, for their high cost and unsustainability in the long term. Previous studies report an intake of 2.5 kg of marine fish to produce 1 kg of salmon [46]. Globally, 1 kg of salmon feed retails at an average price of NOK 13 (€1).

In order to address this challenge, and increase efficiency and sustainability of farmed salmon production, viability lies in diversifying the sources of protein and oils, especially plant sources, in order to reduce exploitation of marine fish species for fish meal and oils, but still retain high nutritional quality of the diets. In this regard, the composition of formulated feeds for salmon has been changing since

1990, with some of the marine ingredients being replaced by ingredients from plant sources [44]. Both fish meal and fish oil composition in salmon feed formulation have declined, with replacement by plant-based ingredients (**Figure 5**). Studies in to alternative feed resources report suitability of zooplankton, mesopelagic fish, some species of squids, and the Antarctic and North Atlantic krill as viable alternatives to fish meal and fish oils [47], as they equally supply excellent levels of omega-3 polyunsaturated fatty acids, vitamins, minerals, essential amino acids, carotenoids and nucleotides. The nutritional composition of such alternative diets is enhanced further by feed additives [47], prebiotics and immunostimulants. Another appealing alternative is the use of by-products and by-catch (non-target fish and other aquatic organisms caught during fishing) from fisheries and aquaculture. This targets the utilization of non-edible parts of fish from processing plants, as well as the discards from fishing expeditions. The use of these materials as ingredients in formulating diets for salmon is strictly undertaken in conformity with the regulations in place, such as the EU regulations on the use of animal products, to control and prevent the spread of diseases and bioaccumulation of contaminants and other undesirable substances [45]. As long as the selection of such materials is done properly, taking in to consideration their nutritional composition, they impart useful nutrients to the feeds formulated for farmed salmon, helping achieve cost-effectiveness, sustainability and high quality of diets, without the use of fish meal and oils [45].

Efforts to find viable alternatives to fish meal and fish oils in feeds for salmon have been concentrated on plant products or ingredients, since their availability, nutritional quality and prices can be achieved competitively. This is underscored by the increasing amounts of plant matter used as ingredients in formulation of feeds for farmed salmon, in comparison with fish meal and fish oils, which are on the decline (**Figure 5** and **Table 2**). In this regard, one of the most suitable and promising plant ingredients is the soy beans as the source of protein and oils, for its high

#### **Figure 5.**

*Trends for raw materials used in feed production for Atlantic salmon in Norway (values in %). Since 1990, vegetable-based ingredients are often used to replace fish meal in feeds for salmon, in order to reduce overexploitation of marine fish species.*

*Perspectives on Salmon Aquaculture: Current Status, Challenges and Genetic Improvement… DOI: http://dx.doi.org/10.5772/intechopen.101531*


#### **Table 2.**

*Norwegian salmon feed ingredients used in 2016 (values in percentage %). In line with the need to reduce exploitation of marine fish meal, ingredients for feed formulation now comprise of 40.2% plant protein sources, while marine protein sources are reduced to about 14.5%.*

protein content, ease of availability and affordability [45]. Other sources of plant ingredients for possible use in formulating diets for salmon include wheat glutten, barley, pea, lupin, corn maize, sunflower, linseed, olive and palm oil. Similarly, vegetable oil is a suitable replacement for fish oils in formulation of feeds for salmon [48]. However, proper attention is required in the choice of the plant material, to ensure that it meets the required amounts of protein, the high amounts of starch in plant matter is adequately reduced, meets suitable profiles for amino acids and minerals, as well as reduced levels of fiber and anti-nutritional factors [45].

The ingredients that constituted the largest portion in Norwegian salmon feed was soy protein content which was 19% and rapeseed oil together with camelina oil accounted for 19.8% while wheat and wheat glutten accounted for 17.9% [44]. The ingredients used in Norwegian salmon feeds in 2016 are as shown in the table below (**Table 2**).

#### **5. Genetics and genomics to support improved breeding of salmon**

Salmon is iconic not only in its ecology, life cycle, ability to oscillate among different environments, high conservation value, but also in its genomic organization. As tetraploid individuals, the genome of salmon evolved through a historical autotetraploidization whole genome duplication (WGD) [49], which occurred 88–103 million years ago [50]. Autotetraploidization occurs by a spontaneous doubling of all chromosomes [5], creating four pairs of chromosomes that recombine spontaneously during meiosis after WGD. Like the normal diploid gametes, there is a reduction in the ploidy state of salmon genome (halfing), a rediploidization process that returns the salmon genome to diploid state prior to recombination [5]. Enormous structural re-organization occurs in the salmon genome during rediploidization, with some parts of the genome remaining tetraploid [51], mismatch in recombination rates of females and males [51], and the retention of half of the genes of the species in duplicated state from the salmonid specific 4th round (Ss4R) of WGD [52]. Apart from this reorganization of the salmonid genome during rediploidization, which creates suitable substrates for the evolution of salmonids, a fifth of salmon genes retained a pair of more ancient gene duplicates from the Teleost specific 3rd round of WGD (Ts3R) [5]. This increases the diversity and complexity of gene families in salmonids, compared to other teleost fishes, which increases evolutionary potential as well as heritability and genetic potential during selective breeding of salmon for commercial aquaculture. The overall effect of these events is a much higher variability in the gene pool, from which samples for generating F1 are drawn.

#### **5.1 Selective breeding in salmon aquaculture**

Selective breeding in support of salmon aquaculture began in Norway, a lead producer of *S. salar* in the 1990s, with the first such programme initiated in 1997, using a total of 40 strains collected across rivers country wide [53]. Concerted efforts produced 4 more strains: Mowi, Rauma, Jakta and Bolaks strains [54], which have been crossed and used extensively, including export to other salmon growing countries. The breeding programme focused on growth rate, with a substantially superior genetic gain per generation of 15% being achieved. This rate is comparatively better than tilapias, where for instance the GIFT strain achieved genetic gain of 12–17% in the fifth generation, compared to 15% in the first generation of salmon [55]. Similarly, in China, the ProGift strain of *Oreochromis niloticus* reported a genetic gain of 11.4% in the 6th generation [56], translating to increased growth of 60–90% bigger body weight at harvest [56]. The high rate of genetic gain in salmon could be attributed to selection intensity, recent history of domestication, in addition to a complex genome following whole genome duplication events [5].

With improved technology and changing interests of salmon breeders in the 1990s, the breeding objectives, moved from growth rate to other complex challenges, such as disease resistance, rationalized by increased incidences of infectious pancreatic necrosis virus (IPNV) for instance [5]. Indeed, disease outbreaks are a major challenge in farmed salmon production in some lead producer countries. To this end, marker assisted selection helped identify individuals with QTL for higher resistance to IPNV [57], resulting to reduced incidence of IPNV, and therefore better yields.

#### **5.2 Genetic mapping**

One of the major challenges facing intensive farming of salmonids is infectious diseases, which often occasion huge losses to farmers, and slows down the rate of expansion of salmon farming. Most of these diseases are caused by bacteria, viruses and parasites [58], whose severity and frequency of occurrence increases with the level of intensification of production. Infectious salmon anemia (ISA), Infectious pancreatic necrosis (IPN), Skeletal muscle inflammation (HMSI), and pancreas disease are viral diseases of salmon [36, 58], which also lower growth rates and increase costs of treatment [58]. The main bacterial disease is the salmon rickettsial syndrome, which causes huge economic losses, while the sea lice disease is the main parasitic disease in farmed salmon. On the other hand, the amoebic gill disease is the main protozoan disease in farmed salmon [59], which also increases susceptibility to other infections. Most of the conventional preventive and prophylactic measures used to control these diseases such as vaccination, antibiotics and antiparasitic drugs, or biosecurity [58], are often not effective. To counter these losses and increase economic returns of salmon farming ventures, selective breeding for resistance to diseases is often applied, based mainly on information from relatives (sib information) [58], since the trait is difficult to measure directly on candidate fish for selection.

#### **5.3 Breeding for disease resistance in farmed salmon**

Global growth of aquaculture is often constrained by progressive loss of quality of the breeding germplasm due to inappropriate fish husbandry as well as selection requisite in particular fish breeding schemes and the repetitive use of certain (good looking or higher yielding) brood stock, and incidences of diseases, especially as production is intensified in pursuit of food security, higher incomes and livelihood.

#### *Perspectives on Salmon Aquaculture: Current Status, Challenges and Genetic Improvement… DOI: http://dx.doi.org/10.5772/intechopen.101531*

Disease resistant fish are those that limit infection by curtailing the replication of the pathogen in the body of the fish [60]. In itself, disease resistance is a precious trait in fish, animal or plant breeding programmes, for it limits wanton use of chemicals or drugs, whose effect is more-broad based, even to non-target organisms in the environment [61], yet their efficacy at limiting incidences and severity of diseases may not be sufficient. Similarly, resistance to drugs or antibiotics by microbes is a real and serious problem in agricultural production [62], exacerbated by global warming [62]. Therefore, alternative, more environment friendly, cost effective and sustainable approaches are desirable in controlling diseases in salmon aquaculture. One of these strategies is the breeding of superior strains, which exploits natural genetic variation for disease resistance to improve the quality, efficiency, profitability and sustainability of the aquaculture enterprise. Today, breeding for improved strains or varieties is a highly efficient process, because of the increasing tool kit of genomic resources, especially for the high throughput next generation sequencing technologies. Therefore, it has been possible to focus on growth, sex determination or disease resistance as breeding objectives [63]. In farmed salmon production, breeding for disease resistant strains is an active agenda since the 1990s [53], since it imparts cumulative and permanent resistance to diseases in the fish. Breeding for resistance nevertheless requires a population of sufficient genetic variation for the trait. High levels of additive genetic variation for disease resistance are reported in different salmonid species (**Table 3**), indicating possibility of deriving gains in selective breeding for disease resistance in salmonids.

Therefore, it is possible to improve resistance to diseases in salmonids through genetic improvement, as a tool in disease control in salmon aquaculture,


**Table 3.**

*Heritability for resistance to different infectious and parasitic diseases in salmonid species. Adopted from [58].*

since heritability for disease resistance is high (**Table 3**) [64–72]. Typically, disease resistance in salmon has been determined through marker assisted selection or genomic selection based only on information from relatives, since it is very difficult to measure disease resistance in the actual fish. By this approach, it is difficult to determine the genetic gain per generation imparted to the fish individuals by the selection effort [58]. This slowed the rate at which selection of disease resistant fish individuals and the realization of highly resistant individuals progresses, since estimated breeding values from sib information is less accurate than would that from the selection candidates themselves [58]. Previous research efforts determined correlation between immune parameters and resistance to diseases in salmon [73]. However, while this may be a pointer to some of the fish individuals that may be resistant to diseases, the total variability in survival of salmon is too low to be attributed to immune variables [58]. Similarly, resistance of fish to diseases is a function of many more factors, and not just immune parameters. Although high genetic variability necessary for improvement of disease resistance exists in salmon, correlations between genetic variation and disease resistance report mixed results [58], with non-existent relationship [72], negative relationship [74], or low to moderately positive relationship [70].

Due to these complexities in studying disease resistance for breeding improved strains for commercial production of salmon, genomic resources have been developed over the last decade, to enable a more focused approach to breeding for disease resistance in salmon. These include: high quality reference sequence for trout, which is also applicable to salmon [52], high density SNP genotyping arrays for *S. salar* [75], and lower density SNP platform for QTL mapping [76]. These resources support the study and understanding of the genetic basis of disease resistance in salmon through identification of candidate genes for resistance to certain diseases, mapping QTL regions with genes of interest for resistance to certain diseases, and gene expression studies [58] in fish challenged with certain pathogens.

#### **5.4 Studying candidate genes driving disease resistance in salmonids**

This approach of understanding disease resistance in aquaculture species exploits the candidate gene theory, in which phenotypic variance for a trait in a population is a result of polymorphisms that exist in genes known to drive that trait [77], and utilizes annotated gene sequences of known function [58]. Due to limited availability of annotated gene sequences in most aquaculture species, studies of association between candidate genes and resistance to diseases has shifted to the Major Histocompatibility Complex (MHC) [58]. The MHC is a multigene family, or a gene-complex region, comprising several genes mediating diverse immune and phenotypic responses or characteristics [78], and interfaces the immune system and pathogens [78]. The MHC presents the class I and II genes, which encode polypeptides that recognize and bind self and foreign peptides and present them to T-cells for destruction [79]. The MHC class I genes bind peptides produced by intracellular degradation of pathogens (such as viruses), and present them to the immune system (cytotoxic T-cells), triggering cellular immune response that destroys the cells. On the other hand, class II genes bind peptides produced outside cells (e.g. bacteria) and present them to helper T-cells, which secrete cytokine mediators. Cytokines elicit humoral (antibody), cytotoxic and inflammatory responses that destroy the pathogens. A unique feature of MHC gene complex is its high levels of polymorphism, with different regions showing high allelic diversity [78]. For instance, *S. salar* from the Baltic Sea has a single MHC class IIB locus with up to 16 alleles within populations [80]. This diversity, thought to be maintained by balancing selection in different taxa, is what makes the MHC a hotbed of scientific interest

#### *Perspectives on Salmon Aquaculture: Current Status, Challenges and Genetic Improvement… DOI: http://dx.doi.org/10.5772/intechopen.101531*

and research. Class I and class II genes are well characterized and highly polymorphic in *S. salar*, and rainbow trout. Association between MHC class IIB alleles and resistance against *A. salmonicida* is reported [81], while variant fish for MHC class I and II are susceptible to IHN [79], but have resistance to furunculosis and ISA [82]. Some salmon fish individuals that bear certain genes in the MHC are more susceptible to furunculosis [81]. These studies seem to suggest that a clear understanding of the MHC and its associated polymorphism can provide useful insights in selecting suitable phenotypes of salmon for breeding for disease resistance, to support intensive and commercial production of the fish. While the number of studies showing correlation of MHC genes to disease resistance and vice versa in salmonids is on the rise, these largely form anecdotal evidence rather than solid evidence for correlation between certain genes of the MHC and resistance to diseases in salmon. This is because resistance to diseases in salmon is a polygenic trait, driven by several genes rather than certain gene(s). Furthermore, the class I genes in the MHC are highly diverse, and this large number of alleles seems to mask the effect of certain alleles, making it difficult to study roles of such alleles in disease resistance or susceptibility. However, since disease resistance traits are typically polygenic, future efforts to understand the genetic basis of disease resistance in salmon should study genetic architecture of variants in the whole genome, as well as possible interactions between genes. Additionally, for populations of salmon where correlation between certain genes and disease resistance or susceptibility has been demonstrated, even where such correlation only seems anecdotal, research should concentrate on studying the suitability of such populations (genotypes) as brood stock for seeds used in selection to improve resistance to diseases. Additionally, loci already identified as having some association with disease resistance should be tested further using modern marker technology, such as next generation sequencing, to improve the confidence of inference.

#### **5.5 Mapping QTL regions for resistance to diseases in salmon**

Quantitative trait locus (loci) (QTL), is the variability of loci, leading to increased variation in the expression of a quantitative character [83]. A QTL is a locus that controls a quantitative phenotypic trait, identified by showing a statistical association between genetic markers surrounding the locus and phenotypic measurements [84]. The presence of QTL improves the understanding of the number of genes and their relative effects in determining expression of the trait. The identified QTL is then mapped through marker association (association mapping) in the whole genome, thereby identifying genomic regions involved in genetic variation of a trait. Fish individuals with the identified QTL or the genomic regions are used in the breeding programme if the QTL is of advantage, or left out if the QTL confers a disadvantage to the fish. SNP markers are especially important in the construction of high-density maps, which are used to fine map QTLs and facilitate identification of causative genes involved in genetic variation for specific characters. SNP markers are available for salmonids [85], and are used in high resolution mapping of disease resistance genes. Since QTL mapping relies on molecular markers, the technique is likely to be used in many breeding schemes, due to the presence of many modern marker technologies, most of which increase the throughput and subsequent output. In this regard, marker technologies like Genotyping by Sequencing (GBS) are already being used in salmon breeding [86]. Coupled with technologies like the Genome wide association studies, these next generation sequencing platforms are likely to accelerate breeding disease resistant salmon strains for use by farmers in commercial aquaculture. These highly versatile NGS platforms enabled the construction of genetic linkage maps, some

incorporating several different markers. GBS has especially opened up new opportunities for genotyping SNPs, which are used to construct dense linkage maps [87], from which genes driving commercially important traits like disease resistance can be deciphered, to aid choice of desirable genotypes for use in the breeding schemes by farmers. For instance, meiotic maps have been developed for sockeye salmon, *O. nerka* [87], suitable for salmonids as tetraploid fishes having duplicated genomes, and which enable comparative genomics and association mapping of important genes or genomic regions of importance in the fish breeding schemes. Analysis of genetic linkage maps aids the location of QTL or genes for important traits for aquaculture production.

In comparative genomics, genomic features in complete genome sequences of different organisms or species are compared. These genomic features vary from DNA sequences, genes, gene orders, regulatory sequences to other genomic structural land marks, that distinguish fish individuals, and can therefore be used to identify suitable genotypes (by comparing regions of similarity and differences) for use in breeding schemes for profitable aquaculture. Autotetraploidization of the common salmonid ancestor 50–120 million years ago [49] made salmonids iconic in character, value and evolutionary potential. As a tetraploid resulting from a duplicated genome therefore, sex determination in salmonids is one of the most complex traits, and probably represents a classic example of diversification in this group of fishes. In itself, tetradiploidization provided evolutionary pressure to diversify species in the Salmonid family in to 11 genera [1]. In this regard, it is interesting to know if sex determination, a trait important for aquaculture, is influenced by the same mechanism for each of the genera within the family, or indeed different mechanisms underpin the process in different genera, or whether different species have different mechanisms, or whether the sex determining gene is the same in the different species, or has shifted to a different chromosome in different species, or whether sex has evolved differently in the different salmonid species that radiated following tetra ploidy. These are uncertainties that have been addressed by comparative mapping, where linkage maps developed for different species are compared, to study the presence or absence of genetic elements of interest, or if these genetic elements are located within different linkage groups or on different chromosomes. Through these comparisons, suitable genotypes are isolated for breeding for the trait of interest.

Through concerted efforts to generate linkage maps for species of salmon, many studies now report sex determining locus on the end of the long arm of chromosome 2. In other species like the brown trout, karyotypic studies report absence of sex determining chromosomes [88]. With this kind of information, gleaned from genetic linkage maps, suitable genotypes can be selected, which when crossed have very high chance of producing monosex seeds, either male or female, depending on which sex is preferred by the farmer. Due to enormous power of linkage mapping in identifying QTLs with important roles in tolerance or resistance of salmonids to diseases that limit intensive and profitable culture of salmon, several such maps have been developed for rainbow trout [89], *S. salar*, *Salmo trutta* [90], the Arctic trout, *Salvelinus alpinus* [91], and Sockeye salmon, *S. nerka* [87]. Apart from these linkage maps from which QTL for tolerance or resistance of salmon for diseases have been inferred, several other studies have also been carried out to improve breeding for disease resistance. For instance, QTL in a back cross of strains of rainbow trout resistant and susceptible to IPN has been detected [92], while QTL for resistance to whirling disease in rainbow trout has been detected [93]. Similarly, with these maps, much more information has been gleaned, such as on which chromosome sex determining genes are located, conservation of synteny, rates of recombination in certain species, loss of genes following autotetraploidization events among

#### *Perspectives on Salmon Aquaculture: Current Status, Challenges and Genetic Improvement… DOI: http://dx.doi.org/10.5772/intechopen.101531*

salmonids and the rate at which such genes were lost, or indeed the emergence of new genetic or sequence features among different salmonid species that radiated following tetraploidization. These research efforts, among a majority of other and ongoing studies, are being incorporated in to breeding schemes by salmon farmers, and demonstrate the importance of salmonids both as high value fish food and sentinel species [94] for human consumption and conservation respectively, and partly explain why farmed salmon production is always on the increase.

On the other hand, association mapping or linkage disequilibrium mapping is the linking of observed phenotypes to the presence of the genotype which drives the observed phenotypic characters or variations [95]. The farmer is interested in seeing the best phenotype from the fish stocked in the ponds or cages or ranches that form his farm, as this translates to higher average tonnage of fish produced and therefore sufficient food for consumption, export and higher profitability of the enterprise. Therefore, to help farmers sustain profitability of their enterprises, researchers try to apply linkage disequilibrium mapping to choose the best genotypes of salmonid species which when used by farmers, give the highest produce, with respect to the trait that the farmer is interested in. As the very basis of Marker assisted breeding, association mapping has hastened identification of suitable genotypes for use in breeding schemes for salmon, addressing a specific breeding objective. In this regard, using RFLP markers, association is reported in backcross families resistant and susceptible to IHN [96]. This means backcross genotypes with RFLP markers show resistance to IHN, while those without RFLP markers are susceptible to IHN, and this easily guides which fish individuals to choose for use in the breeding scheme for resistance against IHN, and which rainbow trout fish individuals to discard, because they lack resistance to IHN. Similarly, AFLP markers associate with resistance to ISA in two full-sib families of *S. salar* [97], with the AFLP markers mapped on to linkage group 8 of the *S. salar* genome [98].

The efforts at comparative mapping and linkage disequilibrium mapping for salmon will be more relevant for precision or more efficient breeding of better performing salmon strains when a large number of markers are available on the map in a clear order, supported by testing of a large number of families (both half sib and full sib) for the presence or lack of important QTLs that associate with certain phenotypes. The studies enumerated above appear disjointed, but will fit better in the international collaboration to sequence the Atlantic salmon genome to be used as the reference sequence for many salmonid species [86] for improved breeding. Furthermore, as more efficient and cost-effective next generation sequencing platforms become available, both genetic high density SNPs marker panels and high-resolution genetic maps are generated, from which association between markers and QTLs for important traits are deciphered [94]. Mapping of these genetic resources on to the reference map generated for *S. salar* [94] facilitates the identification of mutations [58] that underpin disease resistance in many salmonid species and guide precision breeding for improved resistance to diseases for more profitable aquaculture enterprises.

#### **5.6 A study of gene expression for disease resistance**

One of the ways fish resist diseases and therefore some infections do not translate in to full scale sickness is through mounting an immune response to the infection or the pathogen. Related to this immune response are a series of mechanisms that synergize the protective apparatus of the fish. In a population of fish, there will be some individuals with a higher ability to resist pathogens and therefore full manifestation of sickness or symptoms (i.e. resistant fish), and fish that lack ability or do not have sufficient ability to resist pathogens, and therefore develop

the disease (i.e. susceptible fish). Therefore, functional genetic variation for disease resistance will exist in such population of fish [58]. Fish that are resistant to diseases usually show less infection, with fewer viral or bacterial pathogens getting in to the body or cells of the fish. This is because differential immune response in resistant fish inhibits attachment of the pathogen, as well as entry and subsequent replication of the pathogen in fish cells. This inhibition allows the immune system of the fish ample time to mount a sufficient response to completely combat the pathogens [91]. However, should the pathogen succeed to enter the body of the fish, several genes are released by the fish to help fight off foreign invasive agents, with a faster rate of and more intense release in susceptible than resistant fish [99].

For IPNV infection in salmon for instance, interferon induced genes are released to fight the virus. These include Mx, ISG 15, Vip-2, gig 2, and CCL 19 [100]. Additional genes activated to fight IPNV infection in salmon include: Interferon regulatory factor 3 and 8, interleukin 3 receptor, and the macrophage colony stimulating factor, transcription factor 3, and the transcription factor E2-alpha [99]. Similarly, infection with furunculosis stimulates gene expression in response, to help counter-attack the infection. In this regard, Mx1, ubiquitin-protein ligase HERC 4, HERC 5 and HERC 6, ISG 15, eukaryotic translation Initiation factor 4 gamma 1 are elicited during an invasion with ISAV [101]. On the other hand, furunculosis infection in salmon elicits several genes, including JunC, JunD, NFkB, NF-kappaB-105, NFkB1, CYP3A4 and fibronectin [102], which act in different ways and mechanisms to confer protection of the fish against the effects of furunculosis. Since these genes are expressed differently in resistant and susceptible fish, and the fact that in a population of salmon, there are disease resistant and susceptible individuals, resistance has a genetic basis [99, 101, 102]. Therefore, gene expression profiles for disease resistance and susceptibility can help identify suitable fish for use in the breeding programme to improve the resistance of the fish to diseases.

In conclusion, future efforts should focus more on saturating the genetic map for salmon, from which loci for commercially important traits can be inferred, to support breeding efforts for improved strains.

#### **Conflict of interest**

Authors declare no conflict of interest.

#### **Author details**

James E. Barasa\*, Purity Nasimiyu Mukhongo and Cynthia Chepkemoi Ngetich Department of Fisheries and Aquatic Sciences, University of Eldoret, Kenya

\*Address all correspondence to: barkanoti@gmail.com

© 2021 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

*Perspectives on Salmon Aquaculture: Current Status, Challenges and Genetic Improvement… DOI: http://dx.doi.org/10.5772/intechopen.101531*

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#### **Chapter 5**

## Investigation of Trace Metal Bioaccumulation in Wastewater-Fed Fish: A Case Study

*Aslihan Katip*

#### **Abstract**

It was stated that the use of urban wastewater in food production in the 1970s and 1980s may lead to the development of alternative farming systems in the future. Fish fed with wastewater are grown in Asian countries. However, due to the mixing of domestic wastewater with industrial wastewater, many toxic micro-polluting wastewaters affect fish farming even more. The objectives of this study were to investigate the suitability of fish for human food consumption in terms of metals, to provide a basis for the development of a standard on the concentration of heavy metals in reclaimed water used for fish aquaculture, and to search the possibilities of technical improvement of the system in terms of more efficient wastewater treatment. This study will be useful in terms of precautions and disadvantages that can be taken against food shortages that may be experienced with the effect of climate change.

**Keywords:** bioaccumulation, fish, trace metals, transfer factor, wastewater

#### **1. Introduction**

It is estimated that one billion people depend upon freshwater fish as the prime source of protein [1]. Fish consumption makes a major contribution to nutrition, especially for the poorest (e.g., in Cambodia, Laos, and China). Therefore, it is useful to look briefly at the conclusions of the IPCC AR4 on fisheries. Fisheries will come under pressure from increased temperature stress and rising Ph associated with global warming. The frequency of extreme droughts and floods will have a disproportionate effect on fish habitat and populations, and the incidence of diseases is expected to rise. This will result in species extinctions at the margins of their current habitats (e.g., salmon and sturgeon), and fish yields in places like Lake Tanganyika are expected to fall by around 30 percent [2]. Cities will generate increasingly large amounts of effluent that will be recycled for agriculture, subject to water quality and health and safety considerations.

"Water reuse" refers to the production of water through water treatment processes, which introduces a feedback loop in the water cycle. Water reuse presents environmental, economic, and social benefits but also potential drawbacks. Treated wastewater was used in urban uses (green area irrigation, vehicle washing, fire extinguishing, urban pools and toilet water, etc.), industrial (cooling, boiler feeding, process water, etc.), agricultural irrigation, groundwater feeding, direct

or indirect drinking water. Also, it could be used for feeding and improving surface waters and for fish production [3]. The reuse of wastewater for different purposes is even more important these days when there is a danger of drought [4].

#### **1.1 Treatment and advanced treatment applications that could be used for wastewater feeding fishes**

Point and diffuse pollutants are converted into end products such as CO2, N2, H2S, and biomass by being mineralized (decomposed) by natural treatment processes (with the cooperation of bacteria/archae and algae) in rivers, wetlands, estuaries, and seas. A similar separation occurs in wastewater treatment plants [5]. Considering highly treated wastewater as a new water source will become more important in the future, as river flows are predicted to decrease by 20–30% due to global climate change [5]. After the water consumed as drinking/utility water is transformed into wastewater, it can be brought to suitable water quality for different reuse alternatives with the second, third, or advanced treatment stages [6].

Wastewater-fed fish culture has a history of more than a century in Germany. First, it receives well-treated wastewater from wastewater treatment systems. The latter is designed to treat raw wastewater that has been mechanically pretreated only. Net fish yield from wastewater-fed fish ponds is 500 kg/ha/7 months on average (estimated as 860 kg/ha/year), and loading rates are equal to 2000 persons/ha/day [7].

There are still serious psychological, social, and etic hesitations in front of the use of domestic wastewater with advanced treatment, even if it is brought to the quality of tap water, directly as drinking and utility water. It is known that water of this nature is given to aquifers and then drawn by wells and distributed to cities from a separate network (purple network) and used as B quality/class water at 50% lower cost for irrigation, WC flushing water, or industrial process water supply. The most courageous application in which treated wastewater of this quality was used as drinking water in pet bottles, called new water (NEWater), was made in Singapore [8]. The current legislation on the reuse of wastewater in Turkey was published in 2010. "Wastewater Treatment Plants Technical Procedures Communiqué" (Official Gazette no: 27527). In this communique, the selection of treatment technology, design criteria, and technical procedures for reuse of wastewater originating from settlements were given. According to the Communiqué, the main areas of use of treated wastewater were agriculture, industry, aquifer feeding, indirect firewater, use in toilets, and direct drinking water [9].

However, among the areas where treated wastewater can be reused, the most accepted ones are irrigation for agriculture and landscape purposes. The lowest accepted usage areas are direct use in the kitchen and bathroom [10]. Therefore, it is of great importance to increase the low rate of acceptance of the public in using this water, despite the reuse of wastewater by using appropriate engineering techniques [3].

In this case, as the dilution capacity of the streams will decrease, it may be necessary to apply "Ozone Oxidation + Granular Activated Carbon Filtration" at the Advanced Biological WWTP outlet [5]. In the removal of viruses, ultrafiltration membrane application and maturation pools and UV applications for the removal of other pathogenic microorganisms have been determined to provide the desired purification efficiency to a large extent [11]. Smin >3 (1 unit wastewater +2 units river/lake water) criterion can be taken as a measure for the minimum dilution in the discharge of low pollution (gray water or equivalent pollutant) used or treated wastewater into surface waters (streams and lakes). Absolute water should be more than two times of treated wastewater. It is thought that the domestic wastewater that has undergone advanced treatment and disinfection can be mixed with more than two times of clean water and used in the production of aquaculture.

*Investigation of Trace Metal Bioaccumulation in Wastewater-Fed Fish: A Case Study DOI: http://dx.doi.org/10.5772/intechopen.100815*

In this study, trace metal concentrations in muscle, gill, and liver tissues of *Carassius gibelio* specie fed with wastewater from Bursa Water and Sewage Administration East Treatment Place were investigated. Their bioaccumulations and health risks (transfer factors—TF, bio-concentration factors—BCF, and hazard quotient—HQ ) were computed and evaluated by comparison with metal concentrations in wastewater. This study was ensured useful and valuable information for evaluating potential health risks in wastewater recovery as aquaculture feeding water.

#### **2. Materials and methods**

#### **2.1 Study locations**

East Wastewater Treatment Plant treats the wastewater of the eastern part of Bursa City. It covers an area of approximately 250,000 m2 and wastewater of about 1,550,000 inhabitants is mixed with the facility. The 2017 flow rate of the treatment plant is 240,000 m3 /day. It is designed as 320,000 m3 /day for the year 2030. The Wastewater Treatment Plant is discharged into Deliçay Stream, which is a tributary of Nilüfer Stream, in the Susurluk River Basin. The Biological Treatment Plant is a five-stage Bardenphod that removes nitrogen and phosphorus [12].

#### **2.2 Sample handling and analysis of water and fish tissues**

The species *Carrassius gibelio* examined in this study has been recognized as an invasive species by the Republic of Turkey, and its prey has been released throughout the year [13]. The metal concentrations in the muscles, gills, and livers of fish fed with the effluent of the wastewater treatment plant were investigated seasonally. The investigated metals were chosen among the most common ones (Fe, Mn, Cu, Zn, Cr, Pb, Cd, Ni, As, and B) in wastewaters and fish.

Measurements were made by taking three fish samples (*Carrassius gibelio*) in each season in 2011–2012. The sizes of the fishes taken in polyethylene caps were measured in the laboratory. The tissues of muscle, liver, and gill were spared with stainless steel and homogenized. The tissue samples of 0.5 g (wet weight) in petri dishes were dried 24 hours in a drying oven. The samples in which dry weights were obtained were decomposed in a CEM Mars 5 Model microwave device by placing them in HP500 Teflon containers and adding 7 ml of nitric acid (HNO3) and 1 ml of hydrogen peroxide (H2O2) [14]. After filtering, the water samples were acidified with 0.2% (v/v) nitric acid and stored in glass bottles [15]. Water and fish samples were taken and prepared simultaneously.

Trace elements in water and all fish tissues were measured with the ICP-OES device (VISTA-MPX model-VARIAN brand) [16].

#### **2.3 Determination of metal bioaccumulations and risk assessment**

Metal concentrations (based on wet and dry weight) in muscle, gill, and liver tissues were evaluated with national and international standards [17–22].

Transfer and bio-concentration factors (TF and BCF) were calculated to determine the level of bioaccumulation in fish tissues. Transfer factor was used to determine the amount of metal transferred from water or sediment to fish tissues [23]. TF and BCF formulations were given below [23, 24]:

$$\text{TF} = \text{M}\_{\text{tissue}} \left( \text{mg/kg dry weight} \right) / \text{M}\_{\text{sodium or water}} \left( \text{mg/L} \right) \tag{1}$$

$$\text{BCF} = \text{M}\_{\text{tissue}} \left( \text{mg/kg} \,\text{wet weight} \right) / \text{M}\_{\text{water}} \left( \text{mg/L} \right) \tag{2}$$

where Mtissue is the metal concentration in fish tissue; Msediment, metal concentration in sediment. The concentrations in TF sediments were not used in this study because only the effect of water was examined.

BCF is calculated to see the effect of concentrations in water. BCF and TF are inversely proportional to exposure concentrations in the aquatic environment. In international references, it was stated that bioaccumulation was dangerous when BCF was >1000 and TF was >1. BCF and TF should be evaluated together to accurately determine the chronic effects [24, 25].

The consumption of *C. gibelio*, the fish species examined in this study, as the food was determined by the estimated daily intake (EDI) value [26, 27]:

$$\text{EDI} = \frac{\text{Cfish} \, ^\circ \text{Dfish}}{\text{BW}} \tag{3}$$

where Cfish = the average trace element concentration in fish muscle (μg/g dry weight), Dfish = the global average daily fish consumption (g/day) which was only 1.7 g/day for Turkey [28], and BW = average body weight (kg).

The USEPA was stated that the average body weight for an adult human for risk analysis was 70 kg [29]. The Hazard quotient (HQ ) was calculated by dividing the estimated daily intake (EDI) by the established RfD (reference dose) to assess the health risk from fish consumption. It was stated that there was no significant risk when the HQ value was less than 1 [26].

#### **3. Results and discussion**

#### **3.1 Muscle**

Order of magnitude of the metal concentrations in muscle was as follows: Fe > Zn > B > Pb > Ni > Mn > Cu > Cr > Cd > As. It was determined that Mn, Cr, Pb, Cd, and Zn were higher and Cu, Ni, Fe, and As were lower than FAO and WHO standard values. Mn and Zn were determined in lower concentrations compared to Turkish and British standards. Metal concentrations determined in muscle, gill and liver tissues and national-international standard values are given in **Tables 1**–**3**, respectively.

#### **3.2 Gill**

Order of magnitude of the metal concentrations in gill tissue was as follows: Zn > Fe > Mn > B > Pb > Ni > Cu > Cr > Cd > As. Fe, Mn, Zn, Cr, Pb, Cd, and As were determined higher and Cu and Ni were lower than FAO and WHO standards. Mn was lower than Turkish standards. According to Turkish standards, other metals were evaluated similar to FAO/WHO standards.

#### **3.3 Liver**

Order of magnitude of the metal concentrations in liver tissue was as follows: Fe > Zn > B > Pb > Cu > Ni > Mn > Cr > Cd > As. Fe, Mn, Zn, Cr, Pb, and Cd were determined higher and Cu, Ni, As were lower than FAO and WHO standards.

Comparing the Turkish and English standards, Mn and Pb were determined as lower, and other metals were determined similar evaluating FAO/WHO standards.


*Investigation of Trace Metal Bioaccumulation in Wastewater-Fed Fish: A Case Study DOI: http://dx.doi.org/10.5772/intechopen.100815*

#### **Table 1.**

*Metals concentrations determined in muscle tissues and national-international standard values.*


#### **Table 2.**

*Metal concentrations determined in gill tissues and national-international standard values.*


#### **Table 3.**

*Metals concentrations determined in liver tissues and national-international standard values.*

Cd, Ni, As, and B elements determined in muscle, gill and liver tissues, and national-international standard values are given in **Table 4**.

The metal concentrations and accumulation amounts (g/day/body weight) obtained in this study could be used to form a guide value for metal intake. Similar


#### **Table 4.**

*Cd, Ni, As, and B elements determined in muscle, gill and liver tissues and national-international standard values.*

studies should be done with different fish species [27]. The effects of heavy metals on alive changes depending on their concentrations, type of organism, ionic properties of metals (solubility value, chemical structure, ability to form redox and complexes) , tissue in which they are taken into the body and way of intake. Also, other minerals in the ambience and chemical properties of water effect the metal bioaccumulations. Because of these reasons, the physicochemical properties of the water used in aquaculture should be investigated and limited by legal values [30].

#### **3.4 Metal bioaccumulations and risk assessment**

The treated feed wastewater (TFE) was improved with national and international standard values. It was determined that most of the metals examined were above portable water standards [31–33] and USEPA surface water standards for toxic commentating [34]. There is no standard value for Zn and Cu in the Turkish Fisheries Regulation [35]. However, all metals were below the "Irrigation Water of Technical Methods Notification of Wastewater Treatment Plants" [36].

Except for Cd, all the other metals were found below the standard values of the People's Republic of China Fisheries Regulation-GB 8978 [37]. In light of these evaluations, it was been determined that the wastewater fed by the fishes was suitable for irrigation standards but not suitable for some parameters for aquaculture.

Annual and seasonal averages of transfer factors (TF), bio-concentration factors (BCF), and estimated daily intake values (EDI) were computed by using metal concentrations in treated wastewater effluent and examined fish tissues. The calculated factors and values provided a better assessment of the accumulation levels of metals in fish and the health risks that may occur when consumed by humans as


**Table 5.** *The annual averages of metal concentrations in treated effluent and calculated TF, BCF, EDI, HQ values.*

*Investigation of Trace Metal Bioaccumulation in Wastewater-Fed Fish: A Case Study DOI: http://dx.doi.org/10.5772/intechopen.100815*

food. The values of TF, BCF, EDI, HQ, and the annual average metal concentrations of treated effluent are presented in **Table 5**. Computed TF values of all metals in all tissues were determined above the 1. Except for Pb, all other elements were found to be lower than the USEPA BCF limit values. It is known that the TF value gives more realistic results than the BCF values. Large BCF values indicate low chronic effects and low potential for secondary poisoning. In other words, large BCF indicates that there is no high danger. No value can show the hazardous status for BCF values. BCF values of most metals (such as iron) are above 1000 in healthy aquatic ecosystems. Metals have a greater BCF value in systems without contamination. Transfer factors were evaluated since the possibility of coronal effect and the danger status could not be evaluated with BCF [23, 25]. The TF values of all metals examined in this study were found to be above 1. This value shows that metals could bioaccumulate and had potential health effects.

Annual and seasonal averages of TF and BCF values in fish tissues showed that Zn and Fe were high and B and Mn were low values. The order of the annual mean TF and BCF values calculated in the tissues was the same. It was found as Zn > Fe > Pb > Cu > Ni > Cd > As>Cr > Mn > B in muscle, as Zn > Fe > Mn > Pb > Cu > Ni > As>Cr > Cd > B in gill, and as Zn > Fe > Cu > Pb > Ni > Cd > As>Cr > B > Mn in liver. Fe, Zn, and Cu were found to be higher according to the seasonal means of TF and BCF values for the three tissues. Similarities were found in seasonal changes in tissues. According to the calculations for both factors, Cr, Pb, Ni, and B values in muscle were determined as higher in the summer season, Cd was raised in spring, Mn was raised in autumn, and Zn was raised in winter.

Nevertheless, seasonal differences of As, Fe, and Cu elements were found for both factors. BCF values of As, Fe, and Cu were higher in autumn, TF values of As and Fe were higher in summer months, and TF value of Cu was higher in spring. For both factors, Cr, Cd, and Zn values in gill tissues were found higher in spring, Ni and Fe were higher in summer, and Cu was found higher in winter. However, while BCF values of As, Pb, B, and Mn were higher in autumn, TF values of As, B, and Mn were higher in summer months, and TF value of Pb was higher in spring. For both factors, As, Cd, Mn, and Zn values in liver tissues were found higher in autumn, Cr, Cu, and Fe were higher in winter, and Pb and Ni were found higher in spring. However, TF value of B element was higher in summer; BCF value of B was higher in autumn. The annual means of metal concentrations in the tissues were found to differ in the order of magnitude, but according to FAO and WHO standards, the same elements were found to be high (Mn, Zn, Cr, Cd, and Pb) and low (Cu and Ni) in all three tissues. Ni concentrations was over than *C. gibelio* species exist in other water resources. Also, Zn, Cr, and Pb were over than the different fish types. There were differences between the order of magnitude of the concentrations in tissues and the order of magnitude of TF and BCF. While B and Mn concentrations were high in all tissues, the order of bioaccumulation factors of these elements was lower than other elements. Also, the concentrations of Cd and As were lower than other elements; however, their bioaccumulation factors were found higher than the others in all tissues.

It was determined that all elements bioaccumulated in the three tissues according to TF values. TF and BCF values of Fe, Zn, and Cu elements had the highest values in all tissues. The metal concentrations in summer and autumn were higher than in the other seasons. Nevertheless, seasonal differences of bioaccumulation factors were determined distinct from concentration alteration.

The element concentrations apart from B and Fe were determined higher in all tissues in summer, and TF and BCF calculations were determined higher in different seasons. Metal concentrations other than As and B in effluent water

#### *Investigation of Trace Metal Bioaccumulation in Wastewater-Fed Fish: A Case Study DOI: http://dx.doi.org/10.5772/intechopen.100815*

were higher in summer and autumn than in the other seasons like concentrations in fish. Nevertheless, the correlations among the Cd, Mn, Pb, and Cu concentrations in all tissues and effluent water were determined statistically important. The correlations calculated for Cd, Mn, Pb, and Cu elements were found to be significant, indicating that the bioaccumulation was due to effluent. Seasonal changes of other elements' biological accumulation factors and their concentrations in the effluent were found different. Due to these reasons, it was considered that baits and sediment layer of the feeding pool could affect the bioaccumulations in the fishes.

According to EDI and HQ values (**Table 5**), it was observed that there is only a carcinogenic risk in terms of Pb among all metals. Finding the HQ value of Pb greater than 1 indicates a carcinogenic risk. In addition, lead prevents the enzyme systems from working because it imitates the metabolic behavior of the calcium element. Pb is toxic and causes brain damage [29].

#### **4. Conclusions**

The results of these studies showed that the treated wastewater used in fish feeding is suitable for irrigation water, but not for aquaculture. Metal concentrations in the fish tissues were determined as over than the standards. The concentrations of liver and gill were higher than muscle. It was determined that investigated metals (Fe, Mn, Cu, Ni, Zn, Cr, Pb, Cd, As, and B) were bioaccumulated in all tissues. HQ values of Pb element in muscle tissue had carcinogenic risk and BCF value of only Pb among all elements was higher than limit values. It was determined that Pb and Cd, which were the most hazardous metals, were higher than the international regulations. For this reason, it has been determined that the examined fish were not suitable for human and animal edible.

Suggestions for the improvement of this study were presented below:


*Salmon Aquaculture*

### **Author details**

Aslihan Katip Faculty of Engineering, Department of Environmental Engineering, Bursa Uludag University, Bursa, Turkey

\*Address all correspondence to: aballi@uludag.edu.tr

© 2021 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

*Investigation of Trace Metal Bioaccumulation in Wastewater-Fed Fish: A Case Study DOI: http://dx.doi.org/10.5772/intechopen.100815*

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[12] Katip A. Bioaccumulation of Trace Metals in Wastewater-Fed Aquaculture: A Case Study in Turkey Pol. J. Environ. Stud. 2019;**28**(6):4221-4238

[13] Tarkan AS. Yabancı Tatlısu Balıklarının Dünyada ve Türkiye'de Giriş Yolları, Etkileri ve Bunlardan Korunma Yöntemleri. Journal of Fisheries & Aquatic Sciences. 2013;**28**:63-104

[14] Uysal K, Köse E, Bülbül M, Dönmez M, Erdoğan Y, Koyun M, et al. The comparison of heavy metal accumulation ratios of some fish species in Enne Dame Lake (Kütahya/Turkey). Environmental Monitoring and Assessment. 2009;**157**:355-362

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[16] APHA. AWWA Standard Methods for the Examination of Water and Wastewater. 23rd ed. Washington DC USA: American Public Heallth Association; 2017

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[18] FAO/WHO. Evaluation of certain food additives and the contaminants

mercury, lead and cadmium. WHO Technical Report, Series No.505.1989

[19] El-Moselhy KM, Othman AI, El-Azem HA, Metwally MEA. Bioaccumulation of heavy metals in some tissues of fish in the Red Sea, Egypt. Egyptian Journal of Basic and Applied Sciences, I. 2014;**97-105**

[20] Akan JC, Mohmoud S, Yikala BS, Ogugbuaja VO. Bioaccumulation of Some Heavy Metals in Fish Samples from River Benue in Vinikilang, Adamawa State, Nigeria. American Journal of Analytical Chemistry. 2012;**3**:727-736

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[23] Abdel-Baki AS, Dkhil MA, Al-Quraishy S. Bioaccumulation of some heavy metals in tilapia fish relevant to their concentration in water and sediment of Wadi Hanifah, Saudi Arabia. African Journal of Biotechnology. 2011;**10**(13):2541-2547

[24] USEPA. 1999b. Screening Level Ecological Risk Assessment Protocol for Hazardous Waste Combustion Facilities. United States Environmental Protection Agency EPA530-D-99-001C.1999

[25] OECD. Bioaccumulation of Metal Substances by Aquatic Organisms Part 1. OECD Meeting, Paris, September 7-8, 2011

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[27] Ekeanyanwu RC, Nwokedi CL, Noah UT. Monitoring of metals in Tilapia Nilotica tissues, bottom sediments and water from Nworie River and Oguta Lake in Imo State, Nigeria. African Journal of Environmental Science and Technology. 2015;**9**(8):682-690

[28] Sariözkan S. Türkiye'de Balıkçılık Sektörü ve Ekonomisi. Turkish Journal of Aquatic Sciences. 2016;**31**(1):15-22

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[37] ANONYMOUS. National Standard of the People's Republic of China Waste Water Discard Standards.GB 8978-1996, 1996

#### **Chapter 6**

## Sexual Maturation in Farmed Atlantic Salmon (*Salmo salar*): A Review

*Patricia Rivera, José Gallardo, Cristian Araneda and Anti Vasemägi*

#### **Abstract**

The sexual maturation of Atlantic salmon *Salmo salar* is a multifactorial process in which fish acquire somatic characteristics to reproduce. In salmon farming has been described a high variability in the trait age at maturation derived from wild reproductive strategies. Early maturation is a phenotype that generates serious economic repercussions on both, sea cage and on land-based aquaculture systems. In view of the challenges of this problem for the global salmon farming industry, it is essential to thoroughly understand the influencing factors of early and late maturation to find efficient alternatives for managing the phenomenon. This review briefly describes sexual maturation in *S. salar*, its variability in cultures, and the factors influencing the maturation age trait at the physiological, genetic and environmental levels. The control of early maturity through changes to the natural photoperiod and through the use of genetic markers are discussed.

**Keywords:** sexual maturation, *Salmo salar*, multifactorial, reproduction, cultures, variability, photoperiod, physiological, genetic markers, GWAS

#### **1. Introduction**

Sexual maturation in *S. salar* is a complex and multifactorial process whose purpose is to acquire the somatic and behavioral conditions necessary to perform reproductive functions. In both wild and domesticated populations, there is variability in the age at maturation – a characteristic known as a life history trait – which can occur at an early or late stage in both males and females. These reproductive strategies were adopted by wild congeners to increase their reproductive success, perpetuate the species, and promote population sustainability.

Some salmon farms worldwide, including large industries in countries such as Canada [1], land-based aquaculture systems [2], and others, have experienced significant economic losses associated with salmon presenting advanced maturation, either in the freshwater cycle or, with greater repercussions, in fattening stages prior to harvest. These losses occur because when maturation is reached, fish divert energy from body reserves to reproduction, resulting in salmon with a smaller body size and lower organoleptic quality of the fillet. During meat evaluation in processing plants, any degraded physical characteristic will result in a decrease in the commercial value of the fish.

The time and degree of maturation in *S. salar* are influenced by several factors, which can be intrinsic, such as genetic makeup, body composition and metabolic status, or environmental, and these factors can affect anatomical and physiological processes. Among environmental factors, photoperiod is considered a major determinant of the maturation of most cultured teleosts [3], and temperature influences the variation in age and size at maturity in salmonids [4].

Several strategies have been used by the industry to control early maturation in salmon cultures. Among these, photoperiod manipulation has been an alternative that has provided better results in terms of reducing the advanced-maturation phenomenon. Currently, thanks to knowledge regarding the genetic component of sexual maturation, new approaches are being investigated, such as molecular marker-assisted selection. Knowing that the goal of salmon farmers is to maintain salmon in an immature stage to preserve the quality of the product and ensure sustainable production, this review presents a summary of the following topics: life cycle and sexual maturation in *S. salar*; maturation variability in cultures; and physiological, genetic and environmental factors influencing maturation.

#### **2. Life cycle of Atlantic salmon**

Atlantic salmon is an anadromous species whose life cycle (**Figure 1**) in the wild can include a reproduction and rearing phase in freshwater and a growth and sexual maturation initiation phase in the ocean [5, 6]. In this general pattern, there are some alternative strategies, developed mainly by males, that can be very successful in the natural environment, such as, 1) sexual maturation in freshwater as precocious male parr; 2) sexual maturation of fish known as jacks, which mature prematurely in freshwater prior to sea transfer or which reach a body size of approximately 0.5 kg in the sea before maturation [7]; and 3) maturation of fish known as grilse, which reach maturity, with a body size of typically 2 to 5 kg, after 1.5 years in the sea [8] cited in [9]. In all the cases described above, reproduction and spawning occur in the autumn so that the eggs incubate in the gravel substrate during the winter and hatch after two or three months depending on the water

#### **Figure 1.**

*Life cycle of Atlantic salmon. Both males and females of Atlantic Salmon, in the spawning season in autumn, fertilize and incubate eggs which, in spring hatch and will become fries. After a few months, the fries become to be fingerlings, and one to five years after hatching* S. salar *juveniles typically descend as smolts to the ocean to feed and, return to the rivers of origin to a new cycle as adults. Early maturation could be presented in freshwater (precocious male parr); in freshwater prior to sea transfer (jacks), in the first sea winter after transfer to sea (grilse), and in a second or third winter (early maturation). While those adult salmon that mature after 4 or more years in the sea are known as anadromous or late maturing fish.*

temperature [10], so in some environments this process could be delay by the low temperatures of the water. One to five years after hatching, *S. salar* juveniles typically descend as smolts to the ocean to feed and, return with a high degree of fidelity to the rivers of origin to spawn and start a new cycle [11].

#### **3. Maturation in domesticated populations of** *S. salar* **and its implications in production**

The presence of different reproductive and maturation strategies among individuals within a wild population of Atlantic salmon has shown to reflect its genetic diversity [12]. That is, to maintain the natural sustainability of the species, sexual maturation in salmon occurs early or late in different proportions of individuals in both the freshwater and ocean environments [13]. This variability is common and is part of the life history of Atlantic salmon to perpetuate the species and maintain genetic diversity.

Variation in the maturation phenotypes beneficial to population survival in wild populations of Atlantic salmon can be undesirable in domesticated populations. For example, early maturation, especially in fattening stages prior to harvest, affects the profitability of commercial production because it is associated with the expression of secondary sexual characteristics [14]. Losses have also been observed due to the use of body reserves for gamete formation [9] and to decreased growth and degradation of fish meat [15]. These circumstances together hinder not only the profitability of fish farms but also the management, care, and survival of animals [14].

The strong negative impacts caused by the presence of high proportion of early maturing animals are especially noticable in large-scale commercial operations. [2] describe a serious production disaster in a land-based aquaculture system in which 80% of male salmon matured earlier than the harvest time, with recorded weights of 4 to 5 kg, forcing the fish farmers to close their facilities. In economic terms, [1] estimated significant losses of up 4,4% which represented between 11 to \$24 million in 2002 in the salmon industry of New Brunswick, Canada, due to this phenomenon. As noted in both cases, early maturation often has irreparable economic consequences.

The incidence of the early maturation of individuals in domesticated populations is influenced by production goals because the industry seeks to obtain animals with a greater body weight in less time. [1] describe the main risk factors that cause early maturity in salmon; these factors include the intensity of feeding diets with a high fat content, the exaggerated manipulation of photoperiod regimes to delay spawning, and differences in water temperature, among others. As noted, the management of cultures in controlled environments contributes to the risk of early maturation, which is why fish farms find it necessary to resort to other control alternatives.

#### **4. Physiology and factors that influence maturation in Atlantic salmon**

Maturation is a process intrinsically governed by genetic makeup, body composition and metabolic status and by environmental factors [16]. Animals exhibit biological rhythms that are usually in step with environmental factors, which are also known as proximate and ultimate causes or factors [17]. Proximate factors affect anatomical and physiological processes, and ultimate factors underlie adaptation and diversification [18]. Therefore, integration of the totality of these signals in the brain is the main trigger for maturation and reproduction.

Of the environmental factors that can be categorized as proximate, photoperiod is the most important and is considered the main determinant of the maturation of most cultured teleosts [3], it has effects such as delayed onset of sexual maturity in salmonids [16] and increased maturational steroids and gonadal development [19]. In contrast, the temperature influences the variation in the age and size at maturity in salmonids [4] and can alter the time of ovulation [20]. Finally, inter and intraspecific competition maximize reproductive success within the limitations imposed by the opposite sex, the environment and phylogeny [21]. Together, all these factors modulate the maturational and reproductive patterns of salmon. The integration of all these signals when processes in the brain of the fish, especially seasonal changes in the photoperiod, triggers the beginning of maturation and modulates the seasonal patterns of endocrinological activity regulating the cyclic process, whose purpose is to achieve optimal reproduction. Notably, reproductive events occur at times during which salmon determine the survival of their progeny by ensuring the hatching of their larvae in seasons with abundant food resources [22].

In salmonids, the pineal gland and the brain play important roles in the activity of the reproductive axis because they develop light-perceptive, integrative and executive functions [23]. Light perception in these fish occurs through their photoreceptor organs, which transmit an electrical message at night that results from the release of melatonin [24]. The directive derived from this is the secretion of gonadotropin-releasing hormone (GnRH) by hypothalamic neurons and, subsequently, the secretion of gonadotrophins, follicle-stimulating hormone (FSH) and luteinizing hormone (LH), which regulate gametogenesis and gonadal steroidogenesis [3].

The intrinsic factors acting on the physiology of maturation include genetic component. Gene expression of the *vgll3* and variation together with other genomic regions associated with the hypothalamic pathway are analyzed in [25–27]. Based on the results from these studies, it could be suggested the aspects conducive to the maturation process, beginning with the expression of the *ywhab* gene, which contributes to the cytoplasmic retention of the *yap/taz* gene complex, which in turn acts as a cofactor for the expression of the *tead3* gene, ultimately interacting with the *vgll3* gene for the translation of the Vgll3 protein. The vgll3 gene has two alleles; the early maturity allele is expressed in Sertoli cells in males and in granulosa cells in females and acts in cell proliferation processes [27]. However, further research is still needed to understand the biological functions attributed to the genomic regions associated with maturation.

In summary, in a physiological context, sexual maturation can be understood as the process in which an animal begins the development of reproductive competencies through the integration of intrinsic and extrinsic factors. The maturational process is accompanied by a cascade of hormone secretion that modulates gonadal function in specific stages prior to reproduction, where the action of FSH occurs in early stages of gametogenesis, promoting the synthesis of sex steroids for spermatogonial proliferation in males and the progression of vitellogenesis in females and, subsequently, LH acts in the formation of maturational steroids [3].

#### **5. Control of maturation in farmed Atlantic salmon**

During fattening at sea, salmon must be maintained in an immature stage to preserve the quality of the product and ensure a good selling price. Therefore, various strategies have been implemented that help mitigate sexual maturation. For example, a common practice, but only effective in the short term, is eliminating or discarding early maturing males prior to entering the sea. Other alternatives are, for example, those described by [16], who cite, the induction of polyploidy mainly

#### *Sexual Maturation in Farmed Atlantic Salmon (*Salmo salar*): A Review DOI: http://dx.doi.org/10.5772/intechopen.99471*

triploidy, modification of genes and the manipulation of environmental factors, especially photoperiod and temperature as [19]. Finally, recent findings regarding genomic regions that govern sexual maturation in Atlantic salmon [28] have shed light on the genetic determinants of this trait. Next, the use of photoperiod and genetic markers for the control of early sexual maturation is discussed in more detail.

#### **5.1 Control of early maturation by photoperiod in marine cages and land-based aquaculture systems**

Atlantic salmon marine cage aquaculture centers work with photoperiod protocols that seek to reduce the fish's perception of seasonal changes in photoperiod, mainly the decrease in daylight hours from summer to winter, thus inhibiting maturation. Examples of reductions in early maturation in cultures with different photoperiod regimes include the study by [29], who work with one-year-old Atlantic salmon smolts in the northern hemisphere treated with three different photoperiod regimes between January to July, with what, the proportion of sexually maturing fish was significantly lower among both sexes, from 91 to 9% in females and from 74 to 16% in males, in the groups treated from January with natural light + continuous additional light which was not switched off during daytime and was supplied by a 1300-W quartz halogen light. Additionally, in a study by [15], similar results were obtained, with 50% maturation in salmon reared under natural light and only 0.8% in males treated with artificial light for 9 months. More recently, the effectiveness of different alternative sources of artificial light has also been investigated. For example, [30] investigated the incidence of early sexual maturation in a culture of *S. salar* subjected to continuous artificial light, including five different LED light intensities, a single light intensity from a metal halide source and a control treatment with natural light; the results indicated that sexual maturation in males (6.1% under natural light) was arrested uniformly at all intensities. With this, the usefulness of this alternative light source on the control of maturation was confirmed, and widely used in fattening at sea.

The advancement of land-based aquaculture technologies has allowed salmon to complete the life cycle fully in these systems, but early maturation has been reported as a significant problem [19]. To address this issue, several studies have evaluated the efficacy of photoperiod manipulation to control early sexual maturation in these systems. For example, [31] showed that compared with Atlantic salmon exposed to continuous light for 24 hours during the first year, Atlantic salmon exposed to a reduced photoperiod of 18 hours of light from the first feeding to 1 year after hatching in a freshwater recirculation aquaculture system (RAS) showed a significantly higher proportion of mature males despite regimes of photoperiod, so fishes sampled at 19-months, were 50.0% grilse in the 18 h group and 33.3% grilse in the 24 h group. Additionally, [19] showed that the combination of spectral composition, photoperiod and light intensity can be used effectively to suppress or delay the gonadal development of Atlantic salmon reared in RAS. In summary, considerable number of studies demonstrate that photoperiod can be used effectively for the control of early maturation in both marine cages and landbased aquaculture systems.

#### **5.2 Control of early maturation by genetic markers**

Age of maturation in Atlantic salmon is a heritable trait so it should be possible to prevent early maturation using selective breeding [32–34]. Early records of high heritability on age at maturation (0.48 ± 0.20) and therefore great opportunity to

control early maturation in Atlantic salmon were described from the mid-1980s [32]. High heritability values are usually expressed as large differences in the proportion of grilse between families of the same population. However, the systematic elimination of grilse in domesticated populations did not generate the expected results for reasons that will be explained later. This led, during the growth of the Atlantic salmon aquaculture in the 1990s, to the elimination of populations characterized as having high levels of grilse. More recent studies confirm that the age at sexual maturation [14] or some associated traits such as maturation in fresh water [6] or the proportion of grilse [35] have from medium to large heritable component and that there are significant differences between populations.

With the identification of the first genetic markers associated with the age of maturation trait in Atlantic salmon [14, 22], not only has a genetic explanation emerged for the variation previously described in early sexual maturation but foundations have also been laid to initiate more effective control of early maturation through the selection of fish that possess late-maturing genotypes (**Table 1**). The seminal studies of [14, 22], first allowed recognizing that there is a major/effect locus that controls the age of maturation, which has sex-dependent dominance and favors early maturation in males and late maturation in females [22]. This phenomenon may partially explain the great diversity of reproductive strategies observed in *S. salar*, particularly in male precocious parr, jacks and grilses. In addition, this phenomenon may also explain why the phenotypic elimination of early males does not have an impact on the control of early maturation in the long term, as heterozygous females can maintain the early maturation allele and pass it to their offspring. Those authors also identified that the locus with the largest effect on chromosome 25 is associated with the *vgll3* gene (vestigial-like family member 3 gene). This gene explained between 33 and 39% of the variation in age at maturation, an unexpectedly large proportion for a highly complex trait [14, 22].

In addition to abovementioned works, several genome-wide association studies (GWAS) and whole-genome sequencing studies (WGS) have identified additional genetic variants associated with sexual maturation in different wild and domesticated salmon populations. For example, [35], identified another quantitative trait locus (QTL) associated with the age of maturation in North American wild salmon populations; this marker is located on chromosome 6 and explained 6% of the variation in the early maturation phenotype. They also described that the frequency of the early genotype of the *vgll3* gene is lower in this population, contrary to that observed in European populations in which the early genotype is quite common. In turn, [28] reported contrasting results demonstrating that the *vgll3* gene was not associated with maturation in females in a domesticated population, known as Mowi, suggesting that other unidentified genomic regions control the age of maturation. More recently, based on the most extensive GWAS analysis in Atlantic salmon to date, [34] found significant associations with age of maturation in 28 of 29 chromosomes, including two very strong signals that spanned the regions of genes *six6* and *vgll3* on chromosomes 9 and 25, and this study for early maturation demonstrates that using very large sample sizes it is possible to reliably identify loci with small effect.

Regarding the molecular action of these variants on the physiology of maturation, there are several hypotheses related mainly to the *vgll3* gene. *Vgll3* is a regulator of adiposity in vertebrates [38]. Because the fat reserve level is considered a key element in the control of the initiation of maturation [39], its association with the age of maturation in Atlantic salmon seems clear and direct. The *vgll3* gene has two missense mutations strongly associated with age at maturation at amino acids 54 and 323 [14]. The haplotype associated with late maturation (e.g., 3 sea winters) codes for the amino acids threonine (Thr) and lysine (Lys), while those associated with early maturation (1 sea winter) code for methionine (Met) and aspartic acid (Asp). To date, it is unknown how the other markers, such as SNPs found in the *ndufs4*, *rora*,


#### *Sexual Maturation in Farmed Atlantic Salmon (*Salmo salar*): A Review DOI: http://dx.doi.org/10.5772/intechopen.99471*

**Table 1.**

 *Genes associated with age at maturation in wild and domesticated populations of* Salmo salar. *cntn4* genes [34], influence the process of sexual maturation. Therefore, it is essential to continue functional genetic research to fill this knowledge gap in the future.

### **6. Conclusions**

Early maturation is a serious problem for fish farms due to the economic losses, especially in periods close to harvest. Faced with this problem, various control strategies have been used, with photoperiod manipulation on sea cage being widely used in Atlantic salmon. In addition, triggered by fast development of the field of genomics, and based on growing knowledge on genetic components of sexual maturation, the genetic control of maturation is actively being implemented in selective breeding programs. The integration of both strategies should allow progress towards an effective control of early maturation in salmon aquaculture, both in marine aquaculture and in land-based aquaculture.

### **Acknowledgements**

This work was funded by the National Agency for Research and Development (ANID)/Scholarship Program/DOCTORADO BECAS CHILE/2021 – 21211159. This research study also was funded by CONICYT-Chile through project FONDECYT N°1140772 and by the Cooperative Research Program Fellowships of OECD (PCI 2015-CONICYT) awarded to J.A.G.

### **Conflict of interest**

The authors declare that they have no conflicts of interest.

### **Author details**

Patricia Rivera1 , José Gallardo1 \*, Cristian Araneda<sup>2</sup> and Anti Vasemägi3

1 Laboratory of Genetics and Genomics Applied of Aquaculture, Pontificia Universidad Católica de Valparaíso (Pontifical Catholic University of Valparaíso), Chile

2 Faculty of Agronomic Sciences, Department of Animal Production, Laboratory of Genetics and Biotechnology in Aquaculture, University of Chile, Santiago, Chile

3 Department of Aquatic Resources, Swedish University of Agricultural Sciences, Drottningholm, Sweden

\*Address all correspondence to: jose.gallardo@pucv.cl

© 2021 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

*Sexual Maturation in Farmed Atlantic Salmon (*Salmo salar*): A Review DOI: http://dx.doi.org/10.5772/intechopen.99471*

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### *Edited by Qian Lu*

This book discusses the technologies and models of salmon aquaculture. It examines the use of probiotics, the application of recirculation systems, and the addition of highstrength materials in salmon aquaculture. It also discusses the problems hindering the development of salmon aquaculture and proposes potential solutions.

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Salmon Aquaculture

Salmon Aquaculture

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