Fish welfare: an NGO’s point of view

Fish are the most exploited, forgotten and misunderstood animals on the planet. They also are extraordinary creatures: complex, intelligent, sensitive, curious, and some of them have amazing abilities. For instance; some use tools, have a good memory, or collaborate to hunt. And most importantly, they are sentient, and they feel pain. Aquaculture has become the main supplier of fish worldwide, accounting for just over half of the fish eaten by humans due to static global wild-capture stocks, which have been overfished for decades. Also, global consumption of fish has doubled since the early 1970s and will continue to grow with population growth in the developing world. However, the aquaculture industry has developed without proper consideration of the needs of the fish species farmed, and the welfare consequences for those animals. Moreover, the rapid growth of aquaculture has raises major sustainability concerns due to its continued reliance on wild-caught fish. Annually, 0.5-1.0 trillion fish are caught to be reduced to ingredients to feed farmed animals, mainly fish. When considering the negative environmental consequences of using wild-caught fish as feed, we must not overlook the huge animal welfare impact that represents for the huge number of animals involved. Compassion in World Farming is working to raise awareness about fish sentience and the welfare problems that aquaculture industry represents for fish welfare. The way that fish are treated is important and we must do it better.

Palabras clave: bienestar en peces, sintiencia, acuicultura, harina de pescado y aceite de pescado. Introduction Compassion in World Farming (CIWF) is an international animal welfare environmentalist charity. It was funded in 1967 by Peter Roberts, a British dairy farmer who could see first-hand how the demand for "cheap" food was having devastating effect on farm animals, the environment and humans. CIWF focuses on ending factory farming because animal welfare should be a priority in agriculture, and this is not possible with intensive systems. CIWF is working to transform our current food system into one that does not involve cruelty and does not destroy our planet. To achieve these objectives, CIWF is campaigning to strengthen animal welfare legislation, persuading global food companies to produce only higher animal welfare products and exposing the true impacts of factory farming -from animal suffering to environmental pollution, damage to human health and the devastation of our wildlife.
Around the world, up to 2.3 trillion fish are caught from the wild, and up to 167 billion are farmed for human consumption 1 . Of the wild fish captured globally each year, 0.5 -1.0 trillion are caught specifically to feed to farm animals 2 , mostly farmed fish. These wild fish will be reduced to fishmeal and fish oil (FMFO) to produce ingredients for fish feeds. This has allowed the huge growth of intensive aquaculture over the past few decades, an industry that has developed without a proper understanding of the welfare needs of the fish species farmed. Furthermore, most farmed fish are killed without pre-stunning, and suffer slow, painful deaths.
Two years ago, CIWF started a new project focused on fish welfare which has significant potential impact since, of all the animal groups used by humans, fish are by far the greatest in numbers. Fish welfare is gaining more prominence in industry, science and policy, but currently there is much work to be done to ensure that the mental, physical and behavioural need of fish are met in aquaculture. In this rapidly expanding sector welfare impacts on the farmed species are expected, however there are also far reaching impacts on wild animals. In this article, we describe current knowledge of fish sentience and cognition, some key challenges for farmed fish, and present the hidden link to wild fish welfare and ramifications for marine ecosystems.

Fish sentience and cognition
Historically there has been relatively little public concern regarding fish welfare, suggesting a lack of understanding and/or empathy for these animals 3 . Part of the problem seems to be the large communication gap between fish and humans, since we live in different environments which restricts human-fish contact 4 . Fish have unfamiliar body language, have senses that we lack, have no facial expressions that we can understand, and do not make sounds perceivable by the human ear 5 . Therefore, fish do not possess the physical or social characteristics to elicit human empathy or compassion in the way that most other vertebrates do 6 . However, our understanding and perception of fish is progressing. Scientific evidence demonstrates that fish are sentient animals; they are aware of the external environment and of their own internal emotional states, with the ability to experience pleasure, pain and other emotions 7 .
Fish are also more intelligent than we give them credit for 8 . Recent scientific publications document numerous sophisticated behaviours. For example, fish are able to integrate information and have good longterm memories that allow them to learn tasks, problem solve, use tools, cooperate, have numerical skills, navigate long distances and learn through watching others 9 .
Unlike cognitive abilities, what animals feel is more difficult, or even impossible, to measure 10 . We cannot know what is happening inside another animal's mind, even when that animal is another human 11 . Presently, we must rely on brain anatomical traits, and physiological and behavioural responses to identify the capacity for sentience 12 . Teleost (bony) fish have the hardware for pain perception 13 ; they have the necessary receptors (nociceptors) and nerve fibres to detect painful events 14 . Also, they respond to pain relief, e.g. morphine. In fact, they have an opioid system that works in a similar way to mammals' 15 . Not just a reflexive system, fish respond to painful stimuli with physiological and behavioural responses that suggest an emotional and longer-term response 16 . For example, when trout were injected with bee venom or vinegar, their breathing rate increases, stress hormones are released, they lose their appetite and interest in their surroundings, and they appear to focus on the area of the body that has been injured 17 . Higher order cognitive processes such as attention or spatial awareness are significantly altered by the painful stimuli 18 . This demonstrates that fish respond to aversive events and they alter their subsequent behaviour. Despite the evidence mentioned above, there is still controversy surrounding fish pain. The deniers' main claim is that fish cannot feel pain because they do not possess brain structures believed to be essential to conscious pain in mammals, specifically regions of the neocortex and mesocortex. They state that fish show reflexive responses only, and that they are incapable of true cognitive abilities 19 . However, fish have the necessary receptors and nerve fibres to detect painful events and their brains are arranged in a similar structure to mammal brains, with the exception of the neocortex which developed in mammals. Brains of different animals have evolved to do similar things in slightly different ways or using different structures. Another example of this is that in mammals' vision is processed in the 'cortex', but in fish and reptiles' vision is processed in the optic lobe, and yet all of these animals can achieve the same end goal -they can see. Indeed, according to Braithwaite "there is as much evidence that fish feel pain and suffer as there is for birds and mammals" 20 . In any case, there is certainly enough evidence to give fish the benefit of the doubt and treat them with care. It is therefore important that we urgently address fish welfare issues in aquaculture.

Farmed fish
Most of the 51-167 billion fish 21 produced in farms are reared in intensive systems 22 , where fish are kept at high stocking densities in barren environments -a set up tailored to maximise production rather than Appl. Anim. Behav. Sci. 83 (2003)  fish welfare. As for many farmed animals, welfare needs must be met to some extent to achieve good productivity 23 . However, this is usually measured on a group level rather than an individual one (i.e. some individuals may suffer more and there can be a relatively high mortality rate, providing that the system remains economical) and often focus is on the physical health, and less on meeting the mental and behavioural needs of the animal 24 .
In intensive aquaculture fish can suffer from higher rates of acute and chronic stress, aggression and injuries, and with this the risk of disease transmission increases 25 -similar features and problems to those commonly referred to as 'factory farms' for terrestrial animals. Fish are often exposed to extremely stressful handling procedures, involving being taken out of the water where they experience asphyxia, and the vast majority of fish farmed around the globe are killed using inhumane slaughter practices 26 .
Commonly, fish are killed by asphyxiation in air or ice slurry, or exposure to carbon dioxide gas; loss of consciousness and death by these methods is not quick, and suffering is unacceptably prolonged 27 . Alternatively, they may die during the process of gutting and processing 28 . Fish are legally recognized as sentient beings according to the Treaty on the Functioning of the European Union (2012). The Council regulation 1099/2009 on the protection of animals at the time of killing states that " animals shall be spared any avoidable pain, distress or suffering during their killing and related operations", and this statement applies to fish. Therefore, fish should be stunned before being killed to avoid pain and suffering. Stunning methods (such as electrical or percussive stunning) are available and can allow for a more humane death for some species, but there is a significant amount of work required to achieve widespread industry adoption. Other problems that the aquaculture industry should deal with are greenhouse gas emissions 29 , deleterious impacts on wild fish populations from farmed fish escapes (European Comission, 2015), antibiotic and chemical use or abuse 30 , nutrient release from waste feed and faeces that impact the marine environment, and slavery 31 .

Wild-caught fish, fishmeal and fish oil
When considering the negative effects of fish farming, we should not overlook the hidden layer of animal welfare problems: the welfare of wild-caught fish destined for fish feed which fuels aquaculture (and other farmed animals) 32 . That is, the impact of farming carnivorous species 33 . Besides the welfare issues regarding method of production of the farmed fish, we should not disassociate the other fish and marine animals involved in the supply chain 34 . In order to feed many farmed fish species, huge numbers of fish are caught from the wild to be made into feed for farmed fish. 'Reduction fisheries' catch fish and crustaceans (mainly krill) to make fishmeal and fish oil (FMFO), which are the main animal protein ingredients of feeds used for aquaculture and agriculture 35 . Therefore, when assessing the animal welfare impacts of aquaculture, we must include both the farmed fish and the numerous wild-caught fish connected with producing it. We calculated that for the production of one farmed salmon, up to 350 wild-caught fish are used as feed, and so the welfare of those individuals must also be considered 36   immensely during the processes of catching, landing and killing 37 . Industrial fishing methods catch fish in huge numbers at a time. When hundreds of thousands of fish are caught -for example, in a purse seine net or trawling net -they are intensely crowded during capture, then packed tightly together as they are hauled to the surface of the water. Fish will be damaged (e.g. physical abrasions, compression, bursting of internal organs due to sudden pressure changes) and stressed during this process. A significant proportion will die, crushed under the weight of other fish in the nets. For fish that survive capture and landing (being brought aboard the vessel), there is usually no slaughter method; they are simply left to asphyxiate or may die during processing 38 . Marine mammals and birds may also be caught up in these practices, becoming bycatch and dying slow deaths, or being injured during capture and release 39 .
There is also a knock-on effect on marine ecosystems. The fish destined for reduction to FMFO are mainly low trophic level species, plankton feeders that form dense schools. These are often referred to as "forage fish" which includes anchovy, sardine, herring, mackerel, etc 40 . These species play a key role in the marine environment because they transfer energy from primary producers to higher trophic levels such as larger fish, marine mammals and seabirds 41 . Thus, overfishing down food webs can have important ecological impacts for the ecosystem function 42 . While FMFO is generally sourced from reduction fisheries, it also includes fish trimmings and fish is also used directly for feed from by-catch of non-selective fisheries as shrimp trawls 43 . That said, based on FAO fisheries capture tonnages, it is estimated that 0.5-1 trillion fish are caught each year only to be reduced to ingredients to feed farmed animals, mainly fish 44 .
The use of FMFO is supporting the rise of intensive aquaculture which is driven by a growing demand for fish of specific species, mainly carnivorous (e.g. salmon, trout, sea bass, sea bream), that are preferred by consumers in developed countries 45 . On the other hand, many farmed herbivorous species that don't require fish inputs in their feed are increasingly being supplemented with FMFO, or whole fish, to speed up growth 46 . Therefore, the increase in global aquaculture is compromising the future of forage-fish populations, which play a key role in the marine environment, while animal welfare in fish farms remains a major problem. Fortunately, the concept of farmed fish welfare and its importance is starting to gain attention in research, policy and the media. However, the hidden layer to this animal welfare crisis -the welfare of wild-caught fish destined for fish feed -is often overlooked. Together, these industries lead to immense suffering for a huge number of animals.

Proposed improvements
The current food system has become a consumer good, more focused on low prices than in the way that is produced and the true cost of food origin. CIWF believes that we need to move forward to a sustainable and humane food system for people, animals and the environment; a regenerative production system without the cruelty of factory farming. CIWF encourages people to eat less animal products (moderate to low or none) and eat more fresh fruits and vegetables, which is more beneficial to health and the environment than diets heavy in meat, fish, diary, etc 47 .
People who do choose to eat fish may want to look at both sustainability issues and animal welfare.
As a general rule, it may be useful to suggest that people who choose to eat farmed fish to avoid carnivorous fish since huge number of wild-caught fish is used to produce fish feeds. We recommend consuming farmed fish that do not require animal protein in their feed as carp or tilapia. Currently, it is virtually impossible to find "high welfare" fish since inhumane slaughter of fish remains common across the industry. However, some certification schemes have some welfare standards for fish as GlobalGap or BAP. Thus, we encourage consumers to pay attention to fish labels and choose products certified by these schemes. Also, fish produced in extensive or organic production systems are generally reared in better conditions than intensive fish farms as they can be closer to natural environments. For that people who choose wild-caught fish, fish products certified by schemes that ensures sustainable fisheries is recommended (however this does not mean anything for welfare) and it is always better to buy local fish from a small, non-industrial operation.

Conclusions
Here, we have aimed to describe the most important and detrimental issues of fish welfare. The lack of information about fish sentience and cognition resulting in a poor human empathy or compassion has built one of the most important animal welfare problems: the poor value that humans give to fish and therefore, the treatment that they receive from us. A shift in consumer and industry perception of fish is needed to push welfare standards up. Also, research and technical development is needed to meet the wellbeing requirements of the fish. The way forward consists of several steps, which include education, research, transparency from the aquaculture industry, commitment of policies, laws and codes and animal welfare assurance from certification schemes for consumers. Compassion in World Farming is working to spread the message of fish sentience to the general public, consumers, scientists and the whole fish industry because attitudes to fish and the ways that they are treated are important. The numbers of animals affected is huge but also, they are sentient, intelligent and conscious animals and thus capable of suffering. They deserve the same recognition and protection as other groups of animals. It's time to Rethink fish.