Humane Harvesting Initiative: The Influence of Humane Harvesting on Fish Quality, Nutritional Value and Safety

Welfare measurement

As discussed above, the definition of welfare is not clear or straightforward [2]. There are two major issues when it comes to defining and measuring animal welfare [5, 6, 7, 8, 9]. Generating appropriate guidelines for animal welfare depends on resolving these issues. There are differences between terrestrial animals and fish, but the five freedoms developed in the UK regarding terrestrial animals could easily be applied to fish. The five freedoms include freedom from hunger and thirst, freedom from discomfort, freedom from pain, injury, and disease, freedom to express normal behavior and freedom from fear and distress [9]. All five could easily be applied to fish from aquaculture. However, for those harvesting from natural resources like fisheries, it’s more complicated. The five freedoms are applied as a scientifically accurate index for measuring animal welfare [9]. For example, by periodically checking the environment of animals and their physical status within it, their welfare could be determined. However, good animal welfare can go beyond the physical aspects and includes mental changes, which is more complicated when it comes to fish [9]. The concept of animal welfare has been applied to those animals we believe can feel and experience pain, fear, stress and suffering. There is scientific evidence that fish also experience and feel pain, stress and suffering, and that they respond to the stressors in physical, behavioral and physiological scales [10, 11, 12]. Therefore, when fish respond to the stressors, it is hypothetically possible to measure their state of welfare.

Response to Stress

The response to stress starts in the brain and is closely followed by biochemical changes in the blood and subsequent behavioral changes. In aquaculture, the stress could be related to fish crowding, feeding, handling, disease, transportation, drug administration, water quality, temperature fluctuations, harvesting or slaughtering. However, when it comes to fisheries, the stressful conditions are related to pre-harvesting (pre- slaughtering) and slaughtering procedures.The response to stress starts with the release of catecholamines and activation of the hypothalamic–pituitary–interrenal (HPI) axis. Then, corticotropin released from the hypothalamus stimulates the pituitary gland to synthesize and release corticotropic hormones, which then stimulates the synthesis and mobilization of lipid and glucocorticoid hormones (cortisol in teleosts) from the interrenal cells [13, 14]. The energy source mobilization includes the lipid, so changes in plasma-free fatty acids (FFA) could be a stress condition index if not for the fact that the parameter generally does not show a clear response [2]. Secondary and tertiary stress responses, as well as many adverse changes in the quality of the fish, will be initiated by both catecholamines andcortisol [15].

HPI activation results in energy source mobilization, depletion of glycogen stores, and an increase in plasma levels of glucose, along with high muscle activity which can cause anaerobic glycolysis and, as a result, an increase in plasma lactate and a big drop in muscle pH. Therefore, the levels of blood cortisol, glucose and lactate are often used to assess stress levels [16, 17, 18]. It has been shown that through diet modulation, and the use of supplements like vitamin C and vitamin E, the fish’s resistance to stressors will be increased [19, 20, 21]. It cannot, however, be applied for the fisheries industry. Catecholamines (adrenaline and noradrenaline) are not commonly used as stress indicators because they are not easy to determine and are quickly removed from the blood [14]. Cortisol is widely used as both a long-term and short-term stress condition index [22, 23]. While under stress, heart rate will increase and the need for greater oxygen intake will cause a boost in the number of moving erythrocytes and of the hematocrit value, which can also being used as an indicator for stress.A rapid death does not allow a completion of the secondary effects of stress, and pre-slaughter stress always has to be considered in the stress evaluation at slaughter by the hematic parameters.

The effect of Stress on Fish Quality and Nutritional Value

Along with the biochemical changes in plasma due to stress, the texture and nutritional value of the final product will also be adversely influenced by stress and inhumane harvesting practices. Due to stress, the physical movement of muscles will be increased, depleting energy sources, mainly adenosine triphosphate (ATP), and, as discussed above, increasing the lactic acid in muscles and dropping their post mortem pH levels. Hence, those fish which face stressful conditions during harvesting go into rigor mortis rapidly, which negatively effects the quality of the fillets with drip loss and a softening of the muscle texture [24, 25, 26, 27, 28, 29]. Harvesting time is critical for fish in terms of stress, and the amount of stress experienced by a fish depends heavily on the duration, struggle and crowding of the harvesting process. Labored swimming during harvesting causes an intense use of white muscles and results in anaerobic glycolysis followed by increase in lactic acid and less muscle pH (Figure 1).

In contrast, in humanely slaughtered fish, the reduction of stress means that only some muscles will enter rigor mortis while others do not. This difference in timing results in a higher quality fillet in terms of texture. Another physical attribute that can change with harvesting techniques is the color of the fillet. It has been shown that pre-harvesting and harvesting stress significantly affects salmonids fillet color [30, 31] which may be due to the insolubilization of muscle proteins as a result of low pH and drip loss that occurs in the development of prerigor and rigor mortis [32]. In addition, harvesting and post harvesting stress exposes the flesh of fish to the oxidation of polyunsaturated fatty acids (PUFAs), which can result in the production of reactive oxygen metabolites (ROMs). The production of ROMs is proven to induce severe damage in nucleic acid, proteins and lipids, and act as a carcinogen leading to inflammation, glomerular disease and aging for consumers [29, 33, 34, 35, 36]. In fish with a low level of activity, only some muscles have been used. These are the first muscles to enter rigor mortis, while the others do so later. Because of this difference in timing, not all muscles enter rigor mortis at the same time, so the fish as a whole is less stiff [37]. What’s more, stress conditions in harvesting and post harvesting processes can induce peroxidase and aldehyde production in the fish fillet during short storage, which can decrease the nutritional quality of the fish fillet. As a result, the nutrient quality will be decreased, as well as both the texture and flavor of the product due to the degradation and loss of fatty acids and protein. Hence, at the end of the procedure, both physical and nutritional quality will be altered by stress which can influence the marketing to health-conscious consumers. Bagni et al. (2007) [29] found that the ROM was higher in sea bass subjected to stress compared with those kept in normal conditions. One of the major reasons for seafood consumption, particularly marine harvested fish from fisheries, is obtaining the high quality protein and PUFAs. Fish PUFAs have several benefits for humans. They include the ability to decrease blood triglyceride counts, cure rheumatoid arthritis, boostthe effects of antidepressants and combat the depressive symptoms of bipolar disorder. They also help develop the visual and neurological faculties in infants, improve the cognition in children with Attention Deficit Hyperactivity Disorder (ADHD), protect against Alzheimer’s disease and reduce the risk of ischemic stroke, particularly in older people.

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The Relationship between Stress and Food Safety Risk

The relationship between stress and food safety risk has been studied by researchers in animal science. They have found that there is a link between stress and pathogenic bacteria which can increase the food safety risk for humans. The gastrointestinal tract is the main habitat of different bacteria, including both useful and pathogenic bacteria. Technically, the nervous system is controlling the digestive tracts microcirculation, motility and secretions—this is called the brain-gut axis. Since, the first response to stress starts in the brain, it can influence functional and inflammatory disorders as well as infection. Catecholamine hormones particularly norepinephrine are normally presented in the gastrointestinal tract. However, during the stress period, the nervous system of the digestive tract releases catecholamines, causing significant local increases. This increase can strongly influence the intestinal microbial populations. The pathogen can colonize through different methods following stress, including suppression of the immune system, and promoting physiological alterations in the gastrointestinal tract, increasing their virulence and multiplication rate in the gut. Consequently, exposure of farm animals to stressors will lead to increased levels of foodborne pathogens in the gastrointestinal tract and increased risk of contamination of their carcasses [38]. This is important for farmed animals and aquaculture sectors, but it’s worthwhile to predict the stressful conditions in pre-harvesting procedure which might include crowding, duration, and fish movement. The influences of the stress on nutritional value and filet quality were discussed earlier, however, the pre- harvesting and slaughtering methods can influence the microbial growth in fillet too. In 2009, the European Food Safety Authority discussed an opinion related to the influence of farmed fish slaughtering and food safety risk relationship (EFSA 2009). After slaughtering, post- mortem chemical changes begin to take place, including glycolysis, enzymatic activity, nucleotide catabolism, pH drop and an increase in concentration of free non-protein nitrogen (NPN) compounds. The direct relationship between post-mortem changes and fillet quality has been proven, however, these biochemical changes also influence the food safety levels. The level of glycolysis inside the fish at the time of slaughter has a direct effect on the level of NPN, with high levels supporting bacterial growth.

Pre-Harvesting and Harvesting

The term “harvesting” is related to the slaughtering of fish, while “pre-harvesting” includes all activities the fish experiences between catch and slaughter. The term “slaughter,” or “slaughtering,” is used in reference to the termination of an animal life for human consumption. “Euthanasia” is the term used in reference to the humane killing of an animal which is not intended for human consumption. These days, animal slaughtering is an interesting topic for both consumers and the industry, not only in terms of ethics, animal welfare and humane harvesting, but also in terms of the quality, nutritional value and consumer health. Inherently, slaughter is a highly stressful moment for fish [39]. An important part of the slaughter process is decreasing the time between harvesting and slaughtering with fast stunning. Technically, there are two slaughtering methods, fast and slow. Fast methods are being used for big fish, however, it’s not always possible to apply this method for small fish. Some of the slow methods include asphixiation in air, asphixiation in ice, exsanguination, carbon dioxide narcosis, evisceration, decapitation, anesthetics, salt or ammonia bath, anoxic water bath, electro-immobilisation and electro-stimulation as well as electro-fishing [40]. These methods are slow, inhumane and do not promote improved animal welfare. The slaughtering procedure influences on fish welfare could be shown as a model (Figure 2) [41]. In this model, section A shows that fish is killed in an un-humane condition in which fish is conscious, while it should be stunned before that; section B is an ideal condition, in which fish has been stunned and is killed or dies after it is unconscious; in C fish has been stunned but

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it can recover its consciousness and shows un-humane slaughtering; in section D a fish is killed in un-welfare way such as asphyxia while it is conscious but has also suffered from the aversive nature of the stunning method; in section E fish that has been stunned and is killed or dies after it is unconscious but has also suffered from the un- humane stunning method.

Asphixiation or Death in Air

This traditional method for slaughtering fish is based on leaving fish in the air to die. It is the most stressful slaughtering method, with fish experiencing prolonged suffering before death. The death time depends on the hypoxia resistance which is based on on species and temperature.This method is inhumane and can adversely influence the fish quality and shelf life of the products.Some fish, such as eel and carp are resistant to hypoxia, however most other fish are sensitive to hypoxia conditions. Due to the higher metabolism and faster consumption of oxygen, at higher temperatures, death will occur faster once hypoxia sets in. Lower muscle pH, faster rigor mortis and higher muscle lactate were all observed in those fish slaughtered via this method [40, 42].

Asphixiation in Ice

Another method for slaughtering fish is to immediately place them in ice after harvesting. Consequently, the body temperature, metabolic rate, oxygen requirement and movement will all be decreased. The death time is prolonged, however. This method is not humane. Since the death time is prolonged, fish can still feel pain, stress and fear. Hence, it is not recommended [2, 40].

Electrical stunning and electrocution

This method is used for fresh water fish due to the high conductivity of freshwater for stunning with electricity [2, 43]. This method is fast, however, it can cause a violent reaction, including an open mouth and opercula as well as blood spots and other color changes along the backbone muscles. In addition, applying electricity could be harmful for workers.

Bleeding or exsanguination

Many large fish such as tuna and Atlantic salmon are subjected to bleeding by the cutting of gills or veins and left to die in the water. The most common method is bleeding after stunning, however, in many regions, producers use bleeding methods without any pre- stunning method [40]. Bleeding alone is a slow slaughtering method which can induce stress, pain and fear. However, the quality of the final product is high. This method, employed alone, is inhumane. According to the research, there is no scientific evidence which shows that exsanguination without stunning produces a better result than exsanguination after stunning [40]. Studies about the quality of red and white muscles showed that the bleeding of an animal without a heartbeat is similar to the bleeding with a heartbeat [40, 44, 45]. Hence, it is strongly recommended to use bleeding after stunning the fish [40]. There are other slaughtering methods which are fast and more humane, including percussive stunning, hydraulic shock, spiking, shooting and electrical stunning [40].

Percussive stunning

This is one of the most common slaughter methods used in the salmon industry, in cod and halibut fisheries, and by anglers [40, 46]. After removing the fish from the water, a club will be immediately used, either by workers or an automatic machine, to strike the fish’s brain, instantly stunning it. It has been shown that the quality of the fish fillet was higher after applying percussive stunning [40, 47]. Hydraulic stunning This method uses a hydraulic device to stun the fish. However, due to the damage in muscles, the backbone, gut and gas bladder, fish quality will be negatively influenced [40]. Robb, et al.[40] compared different slaughtering methods in terms of humane practice and resulting quality (Table 2). Some of these methods have both low negative impacts on welfare and quality, however, due to some limitations their application is not appropriate. For example, using medicine for fish anesthetics is humane and has a minimal impact on the fish quality, but, due to the regulations, is not recommended. In addition, some other methods such as spiking, shooting and electrical stunning have a low negative effect on welfare and quality, but due to the difficulties in practicing, they are not appropriate methods at an industrial scale. It has been recommended that using two humane methods such as percussive stunning and bleeding not only provides the humane slaughtering aspect, but can also increase the quality of the final products due to the better texture, color and nutritional value. Each of these methods has its own advantages and limitations. In many cases, the method can decrease the stress and increase the fish welfare, but due to the technical demands, cost, low efficiency, and extensive labor required, its application on an industrial scale is not