INTERNATIONALE GESELLSCHAFT FÜR NUTZTIERHALTUNG SOCIÉTÉ INTERNATIONALE POUR LA GARDE DES ANIMAUX DE FERME INTERNATIONAL SOCIETY OF LIVESTOCK HUSBANDRY

NUTZTIERHALTUNGANIMAL HUSBANDRY IMIN FOKUSTHE FOCUS Fish welfare in aquaculture —

Problems TOPICS WINTER 2020

From the research and approaches Researchers discuss current findings in ethology and fish welfare in aquaculture. >> page 4

From the field Practitioners present possible approaches. >> page 60

From the library Introduction to international publication on fish welfare in aquaculture. >> page 79

On animal welfare law / From the jurisdiction The legal situation of animal welfare in farmed fish in Europe and current legal cases in Switzerland. >> page 82

Information brochure of the IGN e.V. about current results from research on animal welfare. EDITORIAL INHALT

Editorial Table of contents

Dear readers, die from the difference in pressure or from Editorial...... 2

being crushed against each other. But even Fishes really are something special. With From the research in pond fisheries, stunning before killing is over 30,000 species, fishes are the largest only mandatory in a few countries. Large Introduction — Farmed fishes: Why so many? Fish welfare: why so late? ...... 4 – 9 and also a very diverse class of vertebrates sections of those involved in fishing or fish Pain and emotion in fishes — Fish welfare Implications for fisheries and aquaculture ...... 10 – 17 that have inhabited almost all aquatic ha- production, as well as specialists and a Sentience in fishes ...... 18 – 22 bitats for over 400 million years. They are dwindling minority of scientists, still hold found in lightless underwater caves, roam Fishes are smart and feel pain: What about joy? ...... 23 – 24 the view that fish suffer ‘stress’ but cannot the high seas, inhabit coral reefs, survive Farming fish: from stress to quality of life and to the dish...... 25 – 29 feel pain. in mud or —like mudskippers —live predo- Coping styles, a tool to better understand fish welfare...... 30 – 36 minantly amphibiously out of the water, It is not easy to prove that fish feel pain. Fish welfare: Interconnections among stress, health, environment and diversity ...... 37 – 39 making the leap to land. Among fishes are The particular difficulty of scientific proof Structural enrichment at fish farms: the science and the fiction ...... 40 – 44 lies in the fact that the prerequisites for the giants like the whale shark and the bas- Knowledge as prerequisite for fish welfare —FishEthoBase as a basis ...... 45 – 55 king shark. Greenland sharks can reach an perception of pain include an emotional Welfare of fish — no longer the elephant in the room ...... 56 – 59 component and a ‘consciousness’ and that age of over 500 years — an unimaginable these factors are difficult to objectify. Scien- period of time for us humans. Fishes have From the field developed organs such as the lateral line tific research on this was therefore lacking organ or possess electrical organs for for a long time. This changed at the begin- Development of fish welfare guidelines for the ‘Friend of the Sea’ (FOS) certification ...... 60 – 64 which there is no equivalent in mammals. ning of the new millennium when a group Fish welfare indicators for the ‘Aquaculture Stewardship Council’ (ASC) standard ...... 65 – 68 They breathe not only with their gills, but of British researchers led by Lynne Sneddon Tasks and working methods of the ‘Aquaculture Welfare Standards Initiative’ ...... 69 – 74 also with their lungs, intestines, skin or their published the results of their investigations Coordination in Swiss aquaculture...... 75 own labyrinth organ. Fishes also recognise on this question, in which they concluded Intensive aquaculture and animal welfare: a practical example ...... 76 – 78 individual conspecifics. Thus, male cichlids that the question about whether fish feel that have observed fights between different pain must be answered with ‘yes’. This trig- From the library conspecifics almost certainly choose the gered a heated and emotional debate that The comprehensive new book of fish welfare ...... 79 loser when it is their own turn to fight. Evi- continues today. It is clear that the econo- Up-to-date overview of fish welfare in aquaculture and animal testing ...... 79 dence that this decision is not made based mic use of fish is considerably facilitated on external characteristics is provided by if one assumes that they do not feel pain. About our relatives under water...... 80 scientific studies in which male fighting fi- Furthermore, intensive research has been Stress and fish welfare: indicators in the mucus...... 80 shes recognised winners and losers only and continues to be carried out in this field Improvement of life regardless of the degree of sentience ...... 81 when they had observed the territorial by various working groups worldwide, and fair-fish: Idea with impact ...... 81 fights themselves. There are fishes that, like various institutions have issued statements groupers, use tools in the form of shells/ on the subject. The evidence for a sense of On animal welfare law / From the jurisdiction stones or form hunting communities with pain, but also for intelligence and even a Fishes in animal welfare law in Europe ...... 82 – 85 other species — abilities that for a long time ‘personality’ is becoming more and more were only attributed to primates. convincing. The fish in Swiss law —current criminal cases ...... 86 – 89

Due to their completely different habitat, I am therefore particularly pleased that From the IGN however, fishes are very alien to most peo- the IGN is dedicating a separate issue to Presentation of an IGN member ...... 90 – 91 ple. They do not have facial expressions fishes. Billo Heinzpeter Studer, together as mammals do and do not make sounds with his colleagues in science and practice, Space for notes...... 92 – 95 when they are in pain. Many vegetarians has compiled a wealth of material on even eat fish. Furthermore, the appearance all aspects surrounding the use of fishes, of fishes does not quite evoke empathy— which allows a completely new view of apart from, of course, the beloved clown- these hitherto very neglected animals. fish Nemo and his friends from the film I hope you enjoy discovering and marvel- ‘Finding Nemo’. ling at these fascinating creatures as you This is probably one of the reasons why look at them with a fresh pair of eyes! fishes are among the most misunderstood A big thanks from the IGN and therefore mistreated creatures. Fishes for their support to: cover a large part of the human protein Johanna Moritz Cover photographs: supply worldwide. Fish farmed in aquacul- Left: Rainbow trouts in a pond (credit: Studer/fair-fish.net) Bavarian State Office for Health Felix Wankel Foundation, ture are ‘harvested’, their stocking density Middle: Sea bream in a net cage (credit: Arechavala-Lopez/FishEthoGroup.net) and Food Safety, Züberwangen, Switzerland given in kilograms/litre of water. In deep- Right: Hatchery for Rainbow trouts (credit: Studer/fair-fish.net) Institute for Animal Health I fair-fish international association, sea fishing, countless fishes suffocate or Denens, Switzerland ISBN: 978-3-9525478-0-9

2 I FISH WELFARE IN AQUACULTURE — I 3 PROBLEMS AND APPROACHES FROM THE RESEARCH

first in modern times to start caring about passion in World Farming for the first time are evolutionarily related and to renounce growth is due to the motivation to create industry, when it knows little about the nat- Introduction — fishes were fishermen and conservationists; in 1992 for farmed salmon [5], the Swiss a self-given special position in the cosmos. an alternative to overfishing of the oceans. ural needs and behaviour of most of these but they were concerned with the preser- association fair-fish from 1997 for edible However, the growth is not the result of col- species? Would it not be wiser, for eco- Farmed fishes: Why so Paradoxically, one reason for the late de- vation of fish species and their habitats, a fish from catch or farming [6], and the lective, governmental decisions, but rather nomic reasons alone, to concentrate on a many? Fish welfare: bate on the welfare of farmed fish may compelling but not sufficient condition for Dutch foundation Vissenbescherming from nothing more than the sum of the decisions few (non-carnivorous) species in order to be the rapid growth of the aquaculture why so late? individual fish. 2000. And it was only in the last decade of many individual entrepreneurs and in- accumulate knowledge? (see Fig. 1) industry, which some environmental or- that many existing or new organisations be- vestors, for whom the prospect of a good ganisations had welcomed for years as Apart from traditional farms, many aqua- Billo Heinzpeter Studer Why did fish welfare become gan to join this commitment. The growing business was and still is the decisive factor. an alternative to the threat of depleting culture industrialists — often career changers an issue so late? attention on the public’s part simultaneously This has several consequences: fair-fish international association the oceans. Consumers probably followed who are betting on a profitable business created the space for an exponential in- Chair: Via delle Giarrette 109, How we relate to the world depends large- the recommendation to buy farmed fish all Firstly, many companies invested and de- as demand grows — are behaving as crease in research in the service of more 34074 Monfalcone, Italia ly on our knowledge of that world. The the more willingly because they could for- veloped when fish welfare was not yet a if they were in a fast new market full of fish welfare. billo @ fair-fish.net popular argument that we know little about get the images from documentaries about widely supported concern and science was niches. The temptation to try something fishes because they live in an element for- Enlightenment is not a continuous process, The fact that the suffering of fishes has only the nasty end of fishes in the fishing indus- only able to say a little about the behav- new seems to be so great that sometimes eign to our species is not entirely valid. at least not as long as the moral varnish of received attention at such a late stage is all try; in aquaculture on land, the fishes are iour and needs of fish — or more precisely: investments are even made without prior Even before the emergence of the modern human civilisation is so thin and easily dam- the more astonishing when one realises that gladly believed to be at least slaughtered of many different fish species. For — sec- market research and production bypasses animal protection movement, individual sci- aged. The relationship of humans towards 93 to 98 % of all vertebrates slaughtered ‘humanely’ … The supposed ecological ondly — in 2014 aquaculture already in- the market; the large marine fish farm in entists had been studying the biology and (other) animals has not developed linearly each year are fishes. While about 70 bil- gain from aquaculture may have diverted cluded 362 fish species, 104 mollusc spe- Völklingen in Saarland failed economically way of life of fishes, as Jonathan Balcombe from a mystical respect that is based on eth- lion land animals are slaughtered every attention from the suffering of the fishes. cies and 62 crustacean species [15]. Of by a hair‘s breadth, and in the case of the reports. One of the fathers of behavioural ical considerations, which move more and year, including poultry [8], according to a It was only when environmental organisa- the 340 aquatic species farmed in 2007, large catfish farm in the Rhine Valley of St. research, Karl von Frisch, proved in an ex- more people today. From the veneration of conservative estimate by the British initia- tions increasingly distanced themselves crit- more than a quarter had only been kept in Gallen, which had to close for other reasons, periment as early as the mid-1930s that at certain animals in pre- and early agrarian tive fishcount, between 1,000 and 3,000 ically from aquaculture, which takes more captivity since 1997, while only a dozen experts doubted whether the large quantity least the dwarf catfish can hear and that, societies, the path led through valleys of billion fishes[9] are killed for us every year fish out of the oceans to feed its farmed species had been farmed before 1900 could have been sold. Why do entrepre- contrary to popular belief, fishes are not lamentation of increasing and religiously (not including other aquatic animals such fish than it ultimately delivers to the West- [14]. Only a few species have been neurs do this to themselves and to fishes? generally deaf. However, an online search sanctioned instrumentalisation of animals. as crabs, squid or mussels), and usually in ern market, characterised by its hunger for farmed for more than 1,000 years: Carp conducted by Balcombe for his book This was until the course of the last century even more brutal ways. predator species [13], that the varnish be- (China), Gilthead sea bream (Mediter- Wild fish would be the smarter ‘What a Fish Knows’ published in 2014 or two, when not only did individual intel- gan to crack, thus also revealing the living ranean), and at best Eel and Trout (Europe) substitute for farmed fish also showed that out of 71 scientific pa- So why has humanity started to care about lectuals rebel against socially organised conditions of the farmed fishes. and Tilapia (Africa). Another driver for the enormous number of pers on the subject of fish welfare, 69 were fish welfare so late? Is it because fishes animal suffering, but gradually an animal are usually found in larger groups and are By comparison, terrestrial livestock farming species in aquaculture is apparently the published after 2001 [4]. Suddenly so many fish — and protection movement arose, at first out of therefore hardly perceived as individuals? has evolved over the last 6,000 to 10,000 retail sector. At a symposium on animal fish species motives of compassion for the animals that Apart from knowledge, there was above That can hardly be the reason; because in years, depending on the species, and has welfare in fish farming at the end of 2016 were nevertheless used, then increasingly all a lack of moral compulsion to deal the industrialised countries of the Western In the meantime, however, aquaculture focused on around 30 species, for good in Zurich [16], industry representatives op- based on a more profound ethic, which with the suffering of fishes. It was only a world, campaigns for farm animal protec- had already grown massively, by 7 to 9 % reasons not including a single predator. posed the strategy propagated by fair-fish today causes a growing number of peo- few centuries ago when it was considered tion often began with laying hens, which annually since the 1950s [14]. Today, it Why does the much younger aquaculture of concentrating aquaculture on a few spe- ple to massively restrict the consumption of quite normal in Europe to regard people also live in groups, usually in very large is still the fastest-growing food industry. It afford itself the luxury of keeping 18 times cies that are most likely to experience wel- products from animal husbandry or to stop of a different skin colour as inanimate and flocks not suited to their species, and are is commonly assumed that this enormous more species than the traditional livestock fare in captivity according to the available it in principle.[1] therefore without rights, therefore free to be thus hardly perceived as individuals. abused, and only in the last century did For a long time, care for the welfare of the realisation gradually break through, in The main reason for society‘s late confron- Table 1: Example of the summary of two FishEthoBase short profiles ‘farm animals’ was left to the farming fam- a society that had been patriarchally dom- tation with the manmade suffering of so ilies, and they were increasingly alone in inated for thousands of years, that women many fishes probably lies in the human Oreochromis Clarias a society that was progressively based on Li Po Ce Li Po Ce should in principle have the same rights as peculiarity of having to reassure itself of niloticus gariepinus the division of labour. It was only with the Li = Likelihood that the individuals men. In both cases, it took the uprisings of a fundamental difference from the animal modern animal welfare movement that con- 1 Home range ? 1 Home range of the species experience welfare slaves and women to promote such reali- world [10]. The Enlightenment has wrested under minimal farming conditions. sumers alienated from primary production sation. It is much more difficult for animals concessions from us time and again; in the 2 Depth range 2 Depth range Po = Potential overall potential of began to care about animal welfare in ag- to protest audibly, but it is particularly diffi- meantime, it is recognised that vertebrates the individuals of the species to riculture from the middle of the last century. 3 Migration 3 Migration experience welfare under improved cult for us to perceive the protest of fishes consciously experience pain, i. e. are sen- This gave rise to protest movements, organ- farming conditions. and animals in general that live under the tient beings, which is why modern animal 4 Reproduction 4 Reproduction isations and political initiatives that led to a Ce = Certainty of our findings in surface of the water. Where the protest protection laws want to protect them ‘as Likelihood and Potential. partial improvement in the living conditions 5 Aggregation ? 5 Aggregation ? of animals is not expressed by refusal to far as is reasonable’ from pain, suffer- of animals in agricultural breeding and fat- grow, by disease or death, and thus under- ing, overburdening, etc. As vertebrates, 6 Aggression 6 Aggression High tening, especially in Western Europe [2], stood by the animal owner at best, it can fishes were tacitly‘included’ , but without with minimum standards at the legal level, 7 Substrate 7 Substrate Medium (not scored in Likelihood) only be expressed by humans. For animal effective consequences; directly applica- such as the phasing out of battery hens [3]. Low species such as hens, pigs or cows, this ble regulations and enforcement principles 8 Stress 8 Stress only emerged in recent times [11]. For a For a long time, even the animal protection has worked since the end of the Second ? Unclear 9 Malformation 9 Malformation movement did not concern itself with the World War with considerable partial suc- long time, fishes were still assigned to a / No findings plight of fish, neither in fisheries nor in fish cess. For the welfare of fishes, on the other grey zone where the sentience remained 10 Slaughter 10 Slaughter ? debatable [12]. It is obviously difficult for farming, neither in experimental laborato- hand, a few organisations only began to FishEthoScore = Sum of criteria scoring humanity to assume that all living beings FishEthoScore 3 8 6 FishEthoScore 0 6 5 ries nor in the numerous home aquaria. The get involved in the 1990s: the British Com- "High" (max. 10)

4 I FROM THE RESEARCH I 5 FROM THE RESEARCH

Table 2: FishEthoScores, domestication level and number of farmed animals, basis: first 43 short profiles knowledge collected in the FishEthoBase of tens of billions per year – a sum that In the practical part, Billo Heinzpeter Stud- [17] (see Fig. 2). A counterargument from could be used to implement sustainable er et al. report on the development of fish Species Li Po Ce Do Animals (in millions) the industry in the final discussion is: with fisheries conversion. welfare criteria and indicators for the Friend a decreasing number of species that can of the Sea (FOS) certification scheme, Nile tilapia Oreochromis niloticus 3 8 6 5 4,900 –15,700 still be sustainably gained from the oceans, Aquaculture is a reality – what based on the FishEthoBase and observa- African catfish Clarias gariepinus 0 6 5 4 160 – 500 aquaculture must ensure diversity in the fish can be done for the fish now? tions on fish farms. Ruth Garcia Gomez supply. This is a remarkable statement from presents parallel work by the Aqua- Yellowtail amberjack Seriola lalandi 4 4 4 2 (20 – 66) Aquaculture is now a reality that must face experts who know more about fish than up to the question of fish welfare. The fol- culture Stewardship Council (ASC) label. Common carp Clarias gariepinus 1 4 2 5 1,700 – 8,700 most consumers. Over 34,000 wild fish lowing articles in this issue present possible Stefan-Andreas Johnigk explains how the Grayling Thymallus thymallus 2 3 0 3 <1 species have been documented [18]; the solutions. Culum Brown and Cat Dorey start German Aquaculture Welfare Standards In- Greater Amberjack Seriola dumerli 1 3 2 2 (20 – 66) number of commercially caught species is from the cognitive abilities of fish and for- itiative intends to improve fish welfare, sup- greater than the number of species farmed plemented by a presentation of the planned European seabass Dicentrachus labrax 0 3 5 5 320 – 400 mulate the consequences in caring for their today. The diversity of supply will continue welfare in aquaculture. Lynne Sneddon coordination office for Swiss aquaculture. Atlantic cod Gadus morhua 1 2 4 4 <1 to come from the oceans, provided that introduces research on pain perception in Finally, Georg O. Herriger shows the con- European perch Perca fluvialtilis 0 2 4 4 <1 –1 their stocks are used wisely! fish, while Becca Franks et al. add to the siderations on fish welfare from the point of view of a fish farming company. Atlantic salmon Salmo salar 1 2 3 5 282 – 659 That aquaculture could replace fisheries is concern for avoiding pain and suffering the Southern bluefin tuna Thunnus maccoyii 1 2 3 3 8 –26 a popular argument. The Kiel fisheries bi- question of how to facilitate positive experi- The fundamental question remains unan- ences for fishes in captivity. Leonor Galhar- Cherry salmon Oncorhynchus masou 0 2 3 4 ? ologist Rainer Froese, one of the fathers of swered so far: which aquaculture with the leading fish database FishBase [18], do then moves from stress avoidance to qua- which species? One possible answer Pacific whiteleg shrimp Litopenaeus vannamei 0 2 3 4 ? dismantled this argument with regard to lity of life, while Maria Filipa Castanheira seems obvious: focus on fish species with Russian sturgeon Acipenser gueldenstadtii 0 2 2 4 <1–1 Europe‘s fish consumption at the aforemen- looks at the relationship between individual a high degree of domestication. However, Siberian sturgeon Acipenser baerii 0 2 0 5 <1–1 tioned symposium: by fishing in a sustain- coping styles and fish welfare (her article an analysis of the first 41 species profiled appeared three years ago in the Fokus is- Grass carp Ctenophayrynqodon idella 0 2 0 5 2,329 –11,646 able way, the yield could be increased in the FishEthoBase shows that the degree by 57 %, so conversely, it is fishing that sue 18 on farm animal personality and has of domestication of a species does not Arctic char Salvellinus alpinius alpinus 1 1 2 5 4 –14 could easily replace aquaculture [19]. This been updated for this issue). Lluis Tort and correlate at all with its potential for high Red porgy Pagrus pagrus 1 1 2 4 1 –3 would spare the suffering of life in captivity Joan Carles Balasch, on the other hand, fish welfare(Fig. 3). This is not surprising, Cobia Rachycentron canadum 1 1 1 4 5 –7 for up to 150 million fish and up to 600 argue for a ‘One Health’ approach, which however; the degree of domestication is starts from health in the sense of healthy Rainbow trout Oncorhynchus mykiss 0 1 4 5 152 –3 ,627 million shrimps per year [20]. The only primarily a measure of the closedness of thing that remains to be solved is the great- habits. Pablo Arechavala-Lopez presents the reproductive cycle in captivity. Many Gilthead seabream Sparus aurata 0 1 3 5 417 – 556 est possible reduction of suffering at the three experiments in which solutions for predatory and other wild animals can also Meagre Arayrosomus reqius 0 1 3 4 14 – 46 abrupt end of their lives in the fishing gear environmental enrichment were tested in be made to reproduce outside their natural Common octopus Octopus vulgaris 0 1 3 3 ? and on board, a question that fair-fish in- fish farms. Jenny Volstorf introduces the Fis- habitat, and at best it is even possible to hEthoBase database, which provides and White sturgeon Acipenser transmontanus 0 1 2 4 ? ternational and its research group will ad- create relatively species-appropriate condi- dress in the future. After all, if you consider interprets ethological knowledge about a tions for them in a zoo. Nevertheless, most Giant tiger prawn Penaeus monodon 0 1 2 4 ? that the stocks of wild fish and aquatic an- growing number of fish species as a pre- of them, and predators in particular, are not Turbot Scophthalmus maximus 0 1 1 3 33 – 93 imals are the last great wild resource for requisite for improving fish welfare. Jo o found in farm animal husbandry. Pikeperch Sander lucioperca 0 1 1 4 1 – 4 human food, it seems downright crazy to L. Saraiva and Pablo Arechavala-Lopez This closes the circle we entered at the overexploit them through ruthless industrial conclude by showing that the welfare of Atlantic sturgeon Acipenser naccarii 0 1 0 4 ? beginning. At the 3rd Summer Shoal exploitation and then want to replace them farmed fish has finally become an issue that Sterlet sturgeon Acipenser ruthenus 0 1 0 4 <1 [22] of fair-fish international, Walter Sán- with farmed animals. But industrial fishing science and practice can no longer avoid chez-Suárez et al. noted that knowledge Burbot Lota lota 0 1 0 3 <1 and aquaculture are subsidised to the tune today. Atlantic halibut Hippoglossus hippoglossus 0 0 5 3 <1 Wreckfish Polyprion americanus 0 0 3 2 ? Table 3: Correlation matrix for selected variables of the FishEthoBase [21]. Barramundi Lates calcarifer 0 0 2 4 38 –255 Brook trout Salvelinus fontinalis 0 0 1 5 1 – 5 Improvement Correlation matrix Likelihood Potential Certainty Domestication Common dentex Dentex dentex 0 0 1 4 <1 Capacity Striped mullet Muqil cephalus 0 0 1 4 10 –30 Likelihood 1 Pangasius Pangasianodon hypopththalmus 0 0 0 3 280 –8 39 Potential 0.60 1 Hybrid sturgeon BAEyNAC, NACxBAE 0 0 0 5 ? Stellate sturgeon Acipenser stellatus 0 0 0 4 <1 Certainty 0.21 0.56 1 Senegolese sole Solea senegalensis 0 0 0 3 1 – 4 Domestication 0.02 0.11 0.14 1 Dover sole Solea solea 0 0 0 3 <1 Improvement Capacity Sharpsnout seabream Diplodus puntazzo 0 0 0 2 <1 –1 0.08 0.80 0.49 0.18 1 Malabar grouper Epinephelus malabaricus 0 0 0 2 <1 First 41 species short profiles. Values are Spearman —›. Signifikant correlations are highlighted. omnivorous mostly carnivorous carnivorous

6 I FROM THE RESEARCH I 7 FROM THE RESEARCH

about fish welfare is still low compared to priate manner and without feed compo- References [14] fish-facts 7: Fischzucht. www.fair-fish. the rapid growth of aquaculture and the nents from forage fisheries. All other fish ch/feedback/mehr-wissen/ [1] Precht R D, 2016. Tiere denken. Vom challenges it creates. While the focus is species can exist in seas, lakes and rivers Recht der Tiere und den Grenzen des Men- [15] FAO, 2016. The State of World on fish health, the provision of husbandry so long as we take care of them. Such a schen. Goldmann, München. 509 Seiten. Fisheries and Aquaculture 2016. Contri- environments that would provide positive recommendation is still anything but popu- ISBN 978-3-442-31441-6. Rezension: buting to food security and nutrition for all. experiences for the fish is neglected. The lar with fish farmers; but as far as fish wel- www.communicum.ch/blog/?p=2531 Rome: FAO. authors suggest using the science of terres- fare is to become a weighty argument for trial livestock welfare as a lens, and using the industry, the development of aquacul- [2] Hürlimann L und Studer B H P, 1997. [16] www.fair-fish.ch/wissen/zucht/fach- its extensive expertise, errors, achievements ture will in the long run not be able to avoid Tiernutz – Tierschutz? 25 Jahre Politik mit tagung-2016/ and methods to better understand the chal- delisting certain species. dem Einkaufskorb. Verlag KAGfreiland, [17] www.fishethobase.net – see the con- lenges and opportunities in studying fish St. Gallen. 112 S. ISBN 3-9521426-0-3 tribution ‘Knowledge as prerequisite for welfare and to develop strategies for filling (beim Autor erhältlich). fish welfare — FishEthoBase as a basis‘ in knowledge gaps. [3] Studer B H P, 2001: How Switzer- this issue. The FishEthoBase, or its FishEthoScore, land got rid of battery cages. https:// [18] www.fishbase.org suggests a different answer: shift towards www.upc-online.org/battery_hens/Swiss the few species with high potential to live Hens.pdf [19] www.fair-fish.ch/wissen/zucht/fach- well in captivity under optimal conditions: tagung-2016/ –> Referat Froese [4] Balcombe J, 2016. What a Fish Knows. As Fig. 2 makes clear, the number of spe- Scientific American, Farrar, Straus and [20] www.fishcount.org.uk/fish-count- cies thus considered is far smaller than the Giroux. ISBN: 9780374714338. See estimates-2 thirty species used in agriculture. The selec- also chapter ‘From the library’ in this issue. tion largely coincides with that based on [21] Saraiva J L, et al, 2019. A ecological considerations, as presented by [5] Lymbery P, 1992, 2002. In Too Deep Global Assessment of Welfare in Farmed Rainer Froese [19]: aquaculture of species – The welfare of Intensively Farmed Fish. Fishes: The FishEthoBase. In: Welfare of that can be farmed in a species-appro- www.eurocbc.org/fz_lymbery.pdf Cultured and Experimental. Fishes 2019, 4 – See also chapter ‘From the library’ in [6] Studer B H P, 2020. FAIR-FISH — Be- this issue. cause You Shouldn’t Tickle Fishes. rüeffer & rub, Zürich. 154 S. ISBN 978-3-906304- [22] www.fishethobase.net/summer-shoal/ 83-0. See also chapter ‘From the library’ summer-shoal2019 — later published as: in this issue. Sánchez-Suárez W, Franks B and Torger- son-White L, 2020. From Land to Water: [7] www.vissenbescherming.nl Taking Fish Welfare Seriously. Animals, [8] Food and Agriculture Organization 10, 1585; doi:10.3390/ani10091585 of the United Nations (FAO). FAOSTAT: Food and Agriculture Data. Last visited in March 2019. www.fao.org/faostat/ en/#home [9] www.fishcount.org.uk [10] Mori B D, Normando S, 2019. Is History Repeating Itself? The Case of Fish and Arthropods’ Sentience and Welfare. Ethics & Politics, XXI, 2. See also chapter ‘From the library’ in this issue. [11] See the contribution ‘The fishes in ani- mal welfare law in Europe’ in this issue. [12] See the contributions ‘Pain and Emo- tion in Fishes’ and ‘Fish welfare: No more the elephant in the room’ in this issue. [13] Tacon A G J and Metian M, 2008. Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: Trends and future prospects. Aquaculture, Volume 285, Issues 1– 4, 146-158.

Trout fattening in raceways, Northern Italy (Photo credit: © Studer / fair-fish)

8 I FROM THE RESEARCH I 9 FROM THE RESEARCH

welfare legislation, while in the Northern context in anticipation that the event will re- stay away. There is little value in detect- returned to feeding after 80 minutes. Clear- their companion. Even more compelling is Pain and emotion in Territory only captive fishes are protected. occur [12] [13]. ing painful stimuli without remembering to ly the painful stimuli reduced the motivation that they spent more time in this zone while fishes — Fish welfare In the remaining states, while fishes are in- avoid them again in future [20]. There must to feed. a shock was being administered and they implications for fisheries cluded in animal welfare legislation, fishing Fish pain be cognitive engagement for the system to remained after the shock, perhaps even activities are exempt, although Tasmanian work. Without cognitive engagement, hav- Case study 2: Pain killers restore further increasing their preference for this and aquaculture One of the reoccurring topics in fish wel- legislation does at least require that fishing fare is whether fishes feel pain. Pain repre- ing just been burnt, you could turn around behaviour sector. This is primarily due to the social is ‘done in a usual and reasonable manner and walk straight back into the fire. The behaviour of fishes which tend to increase 1 sents an emotional experience in response Having shown that fish behaviour changes Culum Brown (Prof.) , and without causing excess’. [38] emotional response to painful stimuli is a their schooling behaviour when threatened 2 to harmful or potentially harmful stimuli and in response to pain, the next obvious ques- Catherine Dorey (Dr.) reinforcer to ensure that we learn from these [26]. Companionship can also buffer emo- One wonders why it is that fishes should is intertwined with the nociception path- tion is to what extent can it be restored if 1  experiences. tional stress [27]. Behavior, Ecology and Evolution of Fishes have such a poor representation in animal way, which is responsible for detecting pain relief is applied. A study [23] exam- Laboratory, Dept. of Biological Sciences, welfare legislation. Even the language harmful stimuli (for example heat). While Since the discovery of nociceptors in fish- ined the change in activity and opercular Collectively these case studies illustrate Macquarie University, Balaclava Rd, associated with fishing (harvest, stocks, there is ongoing debate in this area [14], es there have been considerable research (gill covering) beat rate in rainbow trout 30 that the response to painful stimuli by Macquarie Park NSW 2109, etc.) suggests that they do not qualify as the overwhelming evidence suggests that efforts into studying fish pain in great de- minutes after they were injected subcutane- fishes is not simply reflexive; rather it -in Sydney, Australia, animals, but rather are inanimate objects. fishes do feel pain much like humans [15]. tail. Table 1 shows the accepted criteria for ously with saline, acetic acid, or acetic acid volves long-term cognitive engagement [email protected] One likely answer is that people generally Indeed, the reason humans feel pain at all measuring the capacity of animals to feel combined with pain relief. Injection of acid with pain. The responses made by fishes is because we inherited our pain receptors caused a reduction in activity levels and in- 2 Independent Advisor, Fishes & Fisheries, view fishes as primitive animals with limited pain (modified from[21] and [22]), and in these contexts are not fundamentally and associated cognitive toolbox from a creased breathing rate relative to controls. Science & Policy Campaigns, scope for intelligence. Scientific research in reveals that the evidence for fishes feeling different from those of mammals, and fish ancestor. Nociceptors date back to the Trout injected at the same site as the acid Sydney, Australia the last 20 years, however, has revealed pain is just as good as it is for non-human therefore our own. annelids and emotional responses to pain with the local anaesthetic lidocaine were [email protected] that fishes are much more intelligent than mammals. Furthermore, it is better than that the general public give them credit for [6]. simply act as behavioural motivators [16]. for birds, reptiles and amphibians. It is in- no different from the control trout, suggest- Animal emotions Given the primary role of pain is keeping ing that the pain relief worked and returned Why should we care about In many domains they are as intelligent as teresting to note that the evidence for pain In The Expression of the Emotions in animals safe from harm, it should come as behaviour and physiology back to normal. fish welfare? most land animals [7] [8]. The following in decapod crustaceans and cephalopods Man and Animals, Charles Darwin [28] is a list of the traits reasonably associated no surprise that most animals have this ca- is also comprehensive, and it is unsurpris- These experiments also illustrate the highly Humans interact with fishes in a variety of makes close connections between human with intelligence and, in the not too distant pacity to varying degrees. ing that these taxa are finding their way conservative nature of vertebrate physiolo- contexts and many of these have welfare emotions and their evolutionary precursors past, were once primarily assigned to hu- into animal welfare legislation around the gy, such that many of the drugs designed implications [1]. Fishes are a major source Since the discovery of nociceptors in trout in animals. Darwin proposed that emo- mans: learning and memory, innovation, world. While many of these criteria could for humans also work on fishes. of protein for a significant proportion of the in the early 2000s [17], the debate over tions are adaptive. They serve to motivate social learning, culture, cooperation, rec- whether fishes feel pain has been repeated- arguably be influenced by aspects of the behaviour and also act as a form of com- world’s human population. They remain the Case study 3: Trade-offs between onciliation, nest building, and tool use. ly repositioned [18]. The issue is no longer nociception system only, the last three cate- munication: a means to outwardly express last animals that we largely capture from pain and other motivators Over the last decade or two, all of these gories shown in Table 1 definitely involve wild stocks; however, wild fish populations about whether fishes can detect noxious an animal’s current inner state. At the most behaviours have not only been shown in higher level cognitive processing. Animals Trout were introduced to an aquarium cannot cope with demand and many are stimuli, but rather how they respond on fundamental level, emotions likely guide fishes, but fishes have often led the way as who are in pain show changes in behav- which was divided into three sections. Af- now overfished [3]. In response, aquacul- an emotional level. That is: are they cog- animal behaviour by motivating rewarding model species for understanding these phe- ioural preferences and the choices that they ter acclimation to the tank they showed no ture is increasingly filling the gap. In terms nitively engaged with pain? Rather than behaviour and discouraging behaviour that nomena in non-human animals (for compre- make by, for example, avoiding contexts preferences for any particular sector. When of biodiversity, there are more fish species concentrating on how the human brain results in punishment. Fraser and Duncan hensive reviews of fish cognition see[5] previously associated with noxious events. a mild shock was introduced as the trout than the rest of the vertebrates combined, processes painful stimuli and whether fishes [29] propose that motivational affective [6] [8] [9]). Animals who can experience pain are also entered a sector, they rapidly learned to and freshwater fishes in particular are do something similar [19], let us stop and states evolved to serve two fundamental willing to pay fitness costs to avoid pain by avoid that location after just a few expo- among the most endangered taxa in the The gap between public perception of fish think about why we feel pain at all. That functions: what an animal needs (survival) trading off pain with other fundamental re- sures. Similarly, when a positive reward world [4]. Each of these contexts brings intelligence and scientific reality has seri- is: what is the evolutionary significance of and what an animal wants (opportunism). quirements (for example, access to food or was added to the end of the aquarium unique fish welfare and ethical consider- ous implications for our interactions with pain perception? What is its function? Pain In both cases, the net outcome results in fit- social companionship). This behaviour re- (food or conspecifics) the trout shifted their ations, but to date fishes have largely re- fishes, not least of which is because public perception and the associated emotional ness benefits[30] . Objects or contexts vary veals an ability to titrate the potential dam- space use to access the food or be near mained off the animal welfare radar [5]. opinion can help drive changes in animal response is an ancient, highly conserved in emotional salience. In this way, emotions age caused by noxious stimuli with other their friends. But what happened when the welfare policy and legislation. Intelligence, evolutionary trait [20]. There are two main can help guide animals through the mine- During the 1970s, there was a considera- competing motivators [21] [22]. shock and the reward (food or friends) are sentience and ethics are tied together [5]. components. The first is a simple reflex—an field that is the complex world in which ble increase in advocacy for protecting the placed in conflict? That is: were fishes will- People are far more likely to show empathy emergency move away from a painful stim- they live. By assigning emotions to animals welfare of animals used in industrial agri- The following case studies ing to risk shock exposure to access food or towards animals whom they believe are ulus. No cognition is required as the noci- we assume that they are conscious and are culture (initially in the UK), but for some rea- serve to illustrate the types of friends? When deprived of food for three intelligent [10]. Moreover, animals who ception pathway carries the message from aware of their internal state [31]. son the movement never made it to the sea. experimental evidence that have days [24], or if a companion fish was in are intelligent have greater capacity to suf- the injured limb to the spinal cord before To this day, and as we shall discuss, there contributed to populating table 1 an adjacent compartment [25], fishes trad- Emotions affect the way we interact with fer [11]. This is largely due to their ability the withdrawal order is sent directly back to are few animal welfare controls in aquacul- for fishes. ed-off the risk of shock with the competing the world. They affect our perception and to learn from previous events and project the offending limb. In many cases, there is ture and none in commercial fishing oper- motivator. They were willing to pay a pain decision-making processes. Because of their experience into the future [11]. For no awareness of pain before the withdraw ations. In many countries around the world Case study 1: Pain responses cost to access important resources. this, animal emotions play an important example, if a fish experiences a negative reflex is complete—the brain receives this fishes are not legally defined as ‘animals’ When animals are experiencing pain their role in assessing animal welfare [32]. stimulus (for example, shock or a predator) information afterwards. The second com- The key result in the second experiment under existing animal welfare legislation normal pattern of behaviour changes and Emotions are subjective experiences and in a given context, they rapidly learn from ponent is about long-term consolidation of [25] was from the treatment when a com- or are specifically exempt. In Australia, for pain often takes priority over, or interferes humans rely heavily on verbal reporting of that experience and present signs of fear, that experience. That is, to remember that panion fish was present in the end compart- example, in two states (Western and South with, other motivators. Researchers injected internal states or feelings. Of course, there stress and anxiety when later placed in that object X or context Y is dangerous and to ment. Before the shock, there was a greater Australia) fishes are explicitly excluded from trout in the lips with a noxious substance (ace- are also behavioural and physiological in- preference for the shock zone closest to the tic acid or bee venom) and found that the dices of emotions which we can measure companion. Even though the fishes learnt [33]. Cognitive bias is one such example 1 First published under the title ‘Pain and Emotion in Fishes —Fish Welfare Implications for Fisheries and Aquaculture’ (2019) in: fishes avoided eating for about three hours that they would be shocked in this zone, [34] that has been used as a tool to as- Animal Studies Journal, Vol. 8, No. 2, https://ro.uow.edu.au/asj/vol8/iss2/12/. [17]. In contrast, control fishes and those they still entered the sector to get closer to sess animal emotions and welfare [35]. Courtesy of the publisher and authors (omitting the sections on fisheries). injected with saline (procedural control)

10 I FROM THE RESEARCH I 11 FROM THE RESEARCH

Table 1: Pain Criteria for Animals. Source: adapted from Walters, ‘Defining Pain and Painful Sentience in Animals’ [21]; and Sneddon et al. ‘Defining and Assessing Animal Pain’[22] .

Reptiles/ Criteria Mammals Birds Fishes Cephalopods Decapods Insects Amphibians

Nociceptors, CNS pathways & processing

Analgesic receptor

Physiological responses Figure 1 and 2: Shark fingerlings solving cognition tasks (photo: © Culum Brown)

Pessimists will look at half a glass of wa- in 2018 the global production of ‘fish’ during the period 2001 – 2016. Aquacul- Learned ter and say it is half empty, while optimists (fishes, crustaceans, molluscs and other ture took over from fisheries in 2013 as the avoidance will say it is half full. Animals suffering aquatic animals, but excluding aquatic main supplier of fish for human consump- from poor welfare, for example, tend to mammals, reptiles, and plants) peaked at tion and in 2018 represented 47 % of total demonstrate pessimistic behaviours, such about 178.5 million tonnes. Of the 96.4 fish production and 53 % if non-food uses Change as reduced learning ability [36] [37]. We tonnes of wild-caught fish, 77 % were for are excluded [44]. in behaviour can use our knowledge of how emotions direct human consumption. The remaining Since 1961, the 3.2 % average annual in- interact with cognition to test the welfare 23 % of fish caught, 22.2 million tonnes, crease in global fish consumption has out- status of individual animals. However, this were for non-food uses. In 2016, 15 mil- Protective paced annual human population growth has rarely been done in fishes (but see[38] lion tonnes were processed into fishmeal behaviour (1.6 %) and exceeded the annual increase [39] [40]). This means that we should not and fish oil for feeding farmed fish and oth- in consumption of meat from all terrestrial only focus on preventing poor welfare in er livestock like pigs and chickens, while animals, combined (2.8 %) and indivi- fishes but must actively encourage positive the remainder was utilised as material for Drugs reduce dually, except poultry (4.9 %) [45] welfare. There is increased awareness direct feeding in aquaculture and raising response among animal welfare researchers that just of livestock and fur animals (like mink), to Moreover, according to the FAO, the in- attending to poor welfare does not lead to be cultured (wild juveniles and small adults creasing demand for fish and improve- a lack of suffering [41][42] and there is a caught for on-growing in farms), as bait, ments in technology mean that world fish Self-administration growing movement towards encouraging in pharmaceutical uses, and for ornamental production is expected to expand from of drugs positive welfare states [43]. purposes [45]. 171 million tonnes in 2016, to 201 million tonnes by 2030. Aquaculture is projected A recent study from the University of British Implications for aquaculture to grow 37 % above 2016 levels to reach Pain takes Columbia [46] showed that the FAO Fisheries and aquaculture are by far the 109 million tonnes. [45] priority fisheries landing figures do not reflect the greatest human source of suffering and amount of fish actually caught and killed Fishes as a source of food and painful deaths of fishes, in terms of both the because reporting nations often significant- duration and intensity of suffering inflicted employment Change in behavioural ly underestimate the landings of small-scale and the vast scale of these industries, and In 2015, fish accounted for about 17 % preferences/Choices and subsistence fishers, while recreational hence the number of fishes affected. There catch, discarded bycatch, and catches of animal protein consumed, and provi- are also significant implications in how we from illegal fishing operations are often ded 3.2 billion people with almost 20 % address fish welfare in terms of their impor- of their average per capita intake of ani- Pay cost to not counted. When catch data was recon- tance to humans as a source of food and mal protein [45]. The populations of some avoid pain structed from a wider variety of sources to employment. estimate the numbers missing from official countries eat a lot of fish, in terms of both reports, the authors concluded that global volume and diversity, because they are a The scale of the impact of readily available cultural favourite, while in Trade off pain with catches between 1950 and 2010 were fisheries and farming on fishes other countries people eat a lot because other requirements 50 % higher than those reported to the The Food and Agriculture Organization FAO. they have little choice. In coastal regions of of the United Nations (FAO) collects fish- developing countries, fish is often the only As populations of fishes have declined glob- ing and aquaculture data from member affordable and available source of ani- ally due to overfishing, and catches began countries and produces official statistics on mal protein. In Sierra Leone, for example, to decline after the peak in 1996 [45], the production and use of fishes. In its bien- which has a very low overall food securi- aquaculture grew rapidly to fill the gap in nial report, The State of World Fisheries ty, fish makes up 50 % of the animal pro- demand, with a 5.8 % annual growth rate and Aquaculture [44], FAO estimated that tein consumed. Inhabitants of some island

12 I FROM THE RESEARCH I 13 FROM THE RESEARCH

nations, such as Kiribati and Micronesia in farmed in coastal ponds, and in open cag- during size sorting, vaccination and oth- Despite our knowledge that fishes can suf- and the EU when combined accounted of lives. We recommend reading the sub- the Pacific and the Maldives in the Indian es within lochs, bays, fjords, or the open er veterinary treatments, and harvesting. fer, trillions of fishes [2] are subjected to for approximately 64 % of the total value stantial recommendations on this issue pro- Ocean, depend almost exclusively on fish ocean, and in land-based recirculating Transportation of fishes from hatcheries to inhumane fishing and farming practices an- of world imports of fish and fish products vided by fishcount.org.uk[2] . as a protein source, with consumption rates tanks. Fishes may be farmed throughout grow-out ponds, pens or cages, or be- nually. Many of these practices would not in 2016, or approximately 56 % if trade more than double the global average. the whole life cycle, with eggs produced tween these for cleaning or restocking, is be acceptable to the public if they were within the EU is excluded. in hatcheries, or maybe taken from the wild an especially traumatic experience with applied to animals used within land-based Take Home Message A 150-gram portion of fish provides 50- Farmed fishes must be kept in more natural as eggs, juveniles (like eels) or young adults high loss of life from injury and stress [49] animal agriculture. While there is increas- 60 % of an adult’s daily protein needs and environments at lower densities, and we (most ‘farmed’ bluefin tuna) and grown to [50] [51]. For example, fishes can be ing awareness of the capacity for fishes to contains important fatty acids, vitamins and must find ways to reduce the impacts of han- Scientists have built a significant the required harvest size. pumped from a pond, into a large transport suffer, and the inhumane practices of fish- other essential elements such as iodine and dling and transport [49]. We must choose body of research that shows that tanker, driven to the next facility, and then ing and farming, there has been little action selenium, which do not occur in such quanti- Farms fall into three broad categories—ex- species that cope better with farming and fishes display all the features com- pumped back out again. to date to remedy this. ty and diversity in plant crops or land-based tensive, semi-intensive, and intensive. Exten- that require little in the way of wild fishes in monly associated with intelligence in meat. Thus, fishes are a very important sour- sive systems tend to be the more traditional It is common on salmon farms to find as Various organisations have produced their aquaculture feed. Humane slaughtering mammals, and that they experience ce of nutrition for those with few other op- and sustainable systems which farm under many as a quarter of individuals with stun- guidelines for fish welfare in aquaculture practices must be developed for both indus- stress, fear and pain. These findings tions. In terms of employment, 59.6 million more natural conditions, with low stocking ted growth and abnormal behaviour, often (for example, Humane Slaughter Associa- tries, aquaculture and fisheries. have significant ramifications for people were engaged in the primary sectors densities. Fishes take their nutritional require- floating lifelessly at the surface of the tank. tion), but these often do not address the full animal welfare legislation, an area Despite the overwhelming nature of the of fisheries and aquaculture in 2016: 19.3 ments from the environment, although nutrient They are described as ‘losers’ or ‘drop-outs’, range of welfare issues. Where they are from which fishes have been traditi- problem, there is some room for hope. The million of these in aquaculture and 40.3 rich material may be added to encourage and until recently the cause was unknown. applied on farms, it is primarily to reduce onally excluded. Our most detrimen- rise of campaigns like ‘Meatless Monday’ million people in fisheries. Many millions algae growth for the fishes to feed on. In A recent study showed that the behaviours fish deaths to increase profits, rather than tal interaction with fishes is through and the growing vegetarian and vegan more are employed in fish processing, trade, semi-intensive systems, natural food sources and brain chemistry of these salmon was si- though concern for the full extent of welfare commercial fisheries and aquacul- movements, fuelled by a range of health retail and food services [45]. are supplemented with fertilisers and addi- milar to those seen in stressed and depressed issues. There is little in the way of national ture, an industry that feeds billions of and ethical concerns around meat pro- tional food, such as agricultural byproducts, mammals [52]. They are unable to cope legislation addressing fish welfare. humans and employs millions more. duction, are helpful avenues for reducing How we farm and kill fishes manures, and fishmeal produced from wild with the level of constant and inescapable With growing production in aquaculture, fish consumption. We are seeing a rapid Farmed fishes are under our control fish, which allows higher stocking density. In stress, and essentially give up on life. Fish capture and farm production are report- however, there are distinct opportunities to growth in the development of plant-based for their entire lives, and while the- intensive systems, almost all nutrition is from ed in weight, a fact that significantly deval- When it comes to harvest time, often af- have much greater control over the choice meat alternatives, and lab-cultured meat, re are welfare guidelines available, processed commercial feeds and stocking ues the lives of individual fishes, especially ter a stressful period of starvation to clear of species farmed, and housing conditions with some companies specialising in alter- where these are applied, the goal densities are high. Most of the carnivorous juveniles and smaller species, as well as the out their guts, farmed fishes suffer similar and slaughter methods used, and bring them natives to seafood (for example, sophies is primarily to maximise production species, like salmon, are farmed this way, vast impact of human activities on fishes. Es- inhumane slaughter methods to wild fish- into line with the ethics and welfare require- kitchen.com, finlessfoods.com). and reduce losses, rather than en- and there is a general trend towards more timates based on the FAO’s (under)reported es. Farmed fishes are commonly killed ments for terrestrial agriculture to align more sure good welfare. These industries intensification of aquaculture systems. It is Awareness about the environmental and hu- catch data are that 0.79 to 2.3 trillion fishes by asphyxiation in air or in an ice slurry, strongly with public expectation. However, are important to many of us; how- the high-intensity, high-output farms that have man rights concerns of fish production con- are killed each year by fisheries and another gill-cutting, and carbon dioxide narcosis the drive to increase production could also ever, we need to change these sys- the greatest environmental and human rights tinues to rise, as does the demand by fish 48 to 160 billion by aquaculture [2]. [48] [53] [54] all of which cause con- increase the use of problematic practices, tems to address both welfare and concerns [47] and cause the most suffering traders and retailers for ethically sourced siderable suffering. Some may be gutted such as high stocking densities, that will sustainability. For aquaculture this to fishes, particularly through overcrowding, products. For example, Thai Union, one of The primary concern with regard while alive. The more humane methods of prevent a shift to positive welfare outcomes. means keeping fishes in more natu- handling, transport, starvation, and slaughter the largest fish traders in the world, recently to wild fishes is how we catch percussive stunning (a blow to the head) ral environments at lower densities, [48] [49]. In order to identify priority areas, it may be made significant commitments to address and kill them. and electric stunning methods to render reducing transport and handling helpful to consider the issue of fish welfare unsustainable, illegal, and unethical prac- When it comes to farming – on which we In intensive fish farms, fishes’ physical and fishes unconscious are increasingly being impacts, and choosing species that in terms of the formula used by fishcount. tices throughout its global supply chains are concentrating here –, fishes can suffer mental well-being, and freedom to express used, but only by a minority of farms. These cope better with farming. Aquacul- org.uk [2]: [55]. Addressing fish welfare concerns is throughout their whole life cycle. Fishes are their natural behaviour can be severely com- methods still have some problems (such as ture as well as fisheries need to de- another way that fish producers can dif- farmed in almost as many ways as they are promised by overcrowding in poor condi- inappropriate electrical field strength, and velop humane slaughtering practices. Magnitude of welfare problem ferentiate themselves in the marketplace. fished, from low-intensity backyard ponds tions. Overcrowded fishes, like any animals, poor staff training or conditions) and need = Severity × Duration × Numbers. There is already some common ground be- Fish behaviour and welfare experts that feed Asian households, to high-inten- suffer greater levels of stress and injury, and further development at a species level to will benefit from working with the Given the immense numbers of fishes killed tween fish welfare and industry concerns sity salmon farms in sea cages feeding a have a higher susceptibility to disease [48] ensure humane killing [48] [49] [54]. people and systems that are driving by fishing and farming, we need to begin in that fishes which are reared and killed global demand by the growing middle [49]. Under these conditions the water qual- more ethical and sustainable practi- the process that shifts these industries to- humanely are less stressed, and therefore classes for salmon. ity is often poor, with low oxygen content, Conclusions and a way forward ces in fisheries and farming, to help wards a better outcome for as many fishes produce a better fillet quality and a longer and contaminated with uneaten food, fish Fishes are intelligent, social creatures. The initiate improvements that will benefit We know very little of the ideal require- as possible. This would imply that we must shelf life [56] [57]. waste products including ammonia and car- evolutionary function of pain is ancient and individual fishes and the broader ma- ments for most fishes to live a life where they reduce the demand for fish by addressing bon dioxide, and a variety of chemicals and highly conserved across all vertebrates and Fish behaviour and welfare experts will rine environment, as well as the lives can freely express natural behaviour and the overconsumption by those who do not antibiotics used to combat disease. Fishes likely some invertebrates, and the evidence benefit from collaborating with the people of those working in the industry. We live positive lives, but few farming methods need to eat more animal-based protein. in captivity have no way to avoid stressful for pain in fishes is as good as for mammals. and systems that are driving equitable and must ensure that where we do need provide fishes with a situation close to their Industrialised fish production is primarily situations or environmental changes. They Fishes have neurones for nociception and sustainable practices in fisheries and farm- to farm and capture fishes it is done natural environments to ensure this. This is feeding the expanding seafood consump- cannot escape from other stressed and ag- the necessary brain parts for ‘emotional’ re- ing. Together we can drive improvements humanely, fairly and without unneces- especially true for highly migratory fishes tion of developed and developing coun- gressive fishes, parasites, or predators, and sponses to pain. Fishes engage cognitive- that will benefit individual fishes, and the sary waste of trillions of lives. A sim- like salmons, eels, and tunas. tries. As the FAO report highlights, China cannot seek out cooler or warmer waters, ly in pain perception which has important broader marine environment, as well as the ple way forward would be to reduce is the world’s largest fish consumer (55.9 Freshwater species are farmed in a range or shelter when required. fitness functions. Fishes experience positive lives of those working in the industry. We our reliance on fish as a primary sour- million tonnes, 38 % of global consumption of natural or manmade ponds, channels or and negative emotions which provide in- must reduce our consumption of fish, and ce of protein, particularly in wealthy Intensive farming practices require signif- in 2015 [45] with per capita consumption raceways that are fed by rivers or lakes, sights into their welfare status. We are likely ensure that where we do need to farm and countries where alternatives abound. icant handling of fishes throughout their twice the global average, fuelled by grow- in cages or pens within rivers, or on land- in a position not only to prevent negative capture fishes it is done humanely, fairly lives, and their delicate skin and fins are ing domestic wealth. The other top import- based, closed- system tanks with recircu- welfare in fishes, but also to move towards and without unnecessary waste of trillions often injured when they are transported, ers and consumers of fish, the USA, Japan, lated treated water. Marine species are actively encouraging positive welfare.

14 I FROM THE RESEARCH I 15 FROM THE RESEARCH

References Avoidance Learning Task’. Applied Animal (Carassius auratus) and Trout (Onco- [38] Cerqueira M, et al, 2017. Cogni- [48] Ashley P J, 2007. Fish Welfare: Cur- [58] Links to each State’s legislation are Behaviour Science, vol. 87, pp. 343-54. rhynchus Mykiss) and Implications for Pain tive Appraisal of Environmental Stimuli In- rent Issues in Aquaculture. Applied Animal listed here: https://kb.rspca.org.au/ [1] Huntingford F A, et al, 2006. Current Perception. Applied Animal Behaviour duces Emotion-Like States in Fish. Scienti- Behaviour Science, vol.104, pp.199–235. knowledge-base/what-is-the-australian-leg- Issues in Fish Welfare. Journal of Fish Bio- [14] Sneddon L U, et al, 2018. Fish Sen- Science, vol. 97, pp. 255-71. fic Reports, vol. 7, art. 13181. doi. islation-governing-animal-welfare/ logy, vol. 68, pp. 332–72. tience Denial: Muddying the Waters. Animal [49] Santurtun E, Broom D M, and org/10.1038/s41598-017-13173-x Sentience, vol. 3, vol. 3, no. 21. ani- [26] Brown C and Warburton K, 1997. Phillips C J C, 2018. A Review of Factors [2] Mood A, 2016. Worse Things Happen malstudiesrepository.org/animsent/vol3/ Predator Recognition and Anti-predator [39] Kittilsen S, 2013. Functional Aspects Affecting the Welfare of Atlantic Salmon at Sea: The Welfare of Wild Caught Fish. iss21/1/ Responses in the Rainbowfish, Melanotae- of Emotions in Fish. Behaviour Processes, (Salmo salar). Animal Welfare, vol. 27, www.fishcount.org.uk/published/stand- nia eachamensis. Behavioral Ecology and vol. 100, pp. 153-9. pp. 193–204. ard/fishcountfullrptSR.pdf [15] Sneddon L U, 2015. Pain in Aquatic Sociobiology, vol. 41, pp. 61-8. Animals. The Journal of Experimental Bio- [40] Millot S, et al, 2014. Use of Con- [50] Iversen M, Finstad B, and Nilssen K J, [3] see: Studer, B H P ‘Introduction— logy, vol. 218, pp. 967-76. [27] Culbert B M, Gilmour K M, and ditioned Place Preference/Avoidance Tests 1998. Recovery from Loading and Transport Farmed fishes: Why so many? Fish Balshine S, 2019. Social Buffering of to Assess Affective States in Fish. Applied Stress in Atlantic Salmon (Salmo salar L.) welfare: why so late? In this issue [16] Walters E T, 2018. Nociceptive Bi- Stress in a Group-Living Fish. Proceedings Animal Behaviour Science, vol. 154, Smolts. Aquaculture, vol. 168, pp. 387–94. ology of Molluscs and Arthropods: Evolu- [4] Arthington A H, Dulvy N K, Gladstone of the Royal Society B: Biological Sciences, pp. 104-11. tionary Clues about Functions and Mech- [51] Stien L H, et al, 2013. Salmon Wel- W, and Winfield I J, 2016. Fish Conser- 286 (1910), https://doi.org/10.1098/ anisms Potentially Related to Pain. Frontiers [41] Burn C C, 2017. Bestial Boredom: A fare Index Model (SWIM 1.0): A Seman- vation in Freshwater and Marine Realms: rspb.2019.1626. in Physiology, vol. 9, art. 1049. doi. Biological Perspective on Animal Boredom tic Model for Overall Welfare Assessment Status, Threats and Management. Aquatic org/10.3389/fphys.2018.01049 [28] Darwin C, 1872. The Expression and Suggestions for its Scientific Investi- of Caged Atlantic Salmon: Review of the Conservation Marine and Freshwater Eco- of the Emotions in Man and Animals. gation. Animal Behaviour, vol. 130, Selected Welfare Indicators and Model systems, vol. 26, pp.838–57. [17] Sneddon L U, Braithwaite V A, and John Murray. pp.141-51. Presentation. Reviews in Aquaculture, vol. 5, Gentle M J, 2003. Do Fishes Have No- [5] Brown C, 2015. Fish Intelligence, pp. 33–57. ci-ceptors? Evidence for the Evolution of a [29] Fraser D and Duncan I J H, 1998. [42] Mellor D J, 2016. Moving Beyond Sentience and Ethics. Animal Cognition, Vertebrate Sensory System. Proceedings of ‘Pleasures’, ‘Pains’ and Animal Welfare: the ‘Five Freedoms’ by Updating the ‘Five [52] Vindas M A, et al, 2016. Brain vol.18, pp.1–17. the Royal Society of London. Series B: Bio- Toward a Natural History of Affect. Animal Provisions’ and Introducing Aligned ‘Ani- Serotonergic Activation in Growth-Stunted [6] Brown C, Laland K, and Krause J, logical Sciences, vol. 270, pp. 1115–21. Welfare, vol. 7, pp. 383-96. mal Welfare Aims.’ Animals, vol. 6, p. 59. Farmed Salmon: Adaption Versus Patho- 2011. Fish Cognition and Behaviour. logy. Royal Society Open Science, vol. 3, [18] Rose J D, et al, 2014. Can Fish Re- [30] Balcombe J, 2009. Animal Pleasure [43] Wolfensohn S, et al, 2018. Assess- Wiley-Blackwell. art. 160030. doi.org/10.1098/rsos. ally Feel Pain? Fish and Fisheries, vol. 15, and its Moral Significance.Applied Animal ment of Welfare in Zoo Animals: To- 160030 [7] Bshary R, Wickler W, and Fricke H, pp. 97–133. Behaviour Science, vol. 118, pp. 208-16. wards Optimum Quality of Life. Animals, 2002. Fish Cognition: A Primate’s Eye View. vol. 8, art. 110. doi.org/10.3390/ [53] Robb D H F and Krestin S C, 2002. [19] Woodruff M L, 2018. Pain in Fish: [31] Dawkins M S, 2000. Animal Minds

Animal Cognition, vol. 5, pp.1–13. ani8070110 — see also the chapters ‘Fish- Methods Used to Kill Fish: Field Obser- Evidence from Periphral Nociceptors to and Animal Emotions. Integrative and es are smart and feel pain: What about vations and Literature Reviewed. [8] Vila Pouca C and Brown C, 2017. Pallial Processing. Animal Sentience, vol.3, Comparative Biology, vol. 40, pp. 883-8. joy?’ and ‘Coping styles, a tool to better Animal Welfare, vol. 11, pp. 269-82. Contemporary Topics in Fish Cognition and no.1. animalstudiesrepository.org/anim- [32] Mellor D J, 2012. Animal Emotions, understand fish welfare’ in this issue. Behaviour. Current Opinion in Behavioural sent/vol3/iss21/2/ [54] Van de Vis H, et al, 2003. Is Humane Behaviour and the Promotion of Positive Sciences, vol. 16, pp. 46–52. [44] Food and Agriculture Organization Slaughter of Fish Possible for Industry? [20] Broom D M, 2001. ‘The Evolution of Welfare States. New Zealand Veterinary of the United Nations (FAO), 2020. The Aquaculture Research, vol. 34, pp. 211-20. [9] Vila Pouca C and Brown C, 2018. Pain’. Flemish Veterinary Journal, vol. 70, Journal, vol. 60, pp. 1–8. State of World Fisheries and Aquaculture Fish — How to Ask Them the Right Ques- pp.17–21. [54] Humane Slaughter Association [33] Boissy A, et al, 2007. Assessment of 2020 — Meeting the Sustainable Develop- tions. Field and Laboratory Methods in Ani- (HSA), 2016. Humane Harvesting of Fish. [21] Walters E T, 2018. Defining Pain and Positive Emotions in Animals to Improve ment Goals. UN FAO, Rome, http://www. mal Cognition, edited by N. Bueo-Guerra HSA, UK. www.hsa.org.uk/downloads/ Painful Sentience in Animals. Animal Sen- their Welfare. Physiology and Behavior, fao.org/publications/sofia/2020/en/ and F. Amici, Cambridge University Press, publications/harvestingfishdownload-up- tience, vol.3, no.21. animalstudiesreposi- vol. 92, pp. 375-97. pp. 199-–221. [45] Food and Agriculture Organization dated-with-2016-logo.pdf. tory.org/animsent/vol3/iss21/14/ [34] Harding E J, Paul E S, and Mendl M, of the United Nations (FAO), 2018. The [10] Myers G, 2007. The Significance of [55] Knowles O, 29 May 2018. How [22] Sneddon L U, et al, 2014. ‘Defining 2004. Cognitive Bias and Affective State. State of World Fisheries and Aquaculture Children and Animals: Social Development Greenpeace and Thai Union Turned Up the and Assessing Animal Pain’. Animal Behav- Nature, vol. 427, p.312. 2018. UN FAO, Rome, http://www.fao. and Our Connections to Other Species, Heat on the Tuna Industry. News Deeply. iour, vol. 97, pp. 201-12. org/publications/sofia/2018/en/ 2nd edition, Purdue University Press. [35] Mendl M, Burman O H P, Parker [56] Borderias A J and Sanchez- [23] Mettam J J, Oulton L J, McCrohan C R, R M A, and Paul E S, 2009. Cognitive Bias [46] Pauly D and Zeller D, 2018. Catch [11] Bekoff, M, 1994. Cognitive Ethology Alonso I, 2011. First Processing Steps and Sneddon L U, 2011. The Efficacy of as an Indicator of Animal Emotion and Wel- Reconstructions Reveal that Global Marine and the Treatment of Non-Human Animals: and the Quality of Wild and Farmed Fish. Three Types of Analgesic Drugs in Reducing fare: Emerging Evidence and Underlying Fisheries Catches are Higher than Reported How Matters of Mind Inform Matters of Journal of Food Science, vol. 76, pp. Pain in the Rainbow Trout, Oncorhynchus Mechanisms. Applied Animal Behaviour and Declining. Nature Communications, Welfare. Animal Welfare, vol. 3, no. 2, R1–R5. doi.org/10.1111/j.1750-3841. mykiss. Applied Animal Behaviour Science, Science, vol. 118, pp. 161-81. vol. 7, art. 10244. doi.org/10.1038/ pp. 75–96. 2010.01900.x vol. 133, pp. 265-74. ncomms10244 [36] Destrez A, et al, 2013. Chronic Stress [12] Chandroo K P, Duncan I J H, and [57] Digre H, et al, 2017. The On-Board Live [24] Millsopp S and Laming P, 2008. Induces Pessimistic-Like Judgment and [47] Allsopp M, Santillo D, and Dorey Moccia R D, 2004. Can Fish Suffer? Per- Storage of Atlantic Cod (Gadus Morhua) Trade-offs Between Feeding and Shock Learning Deficits in Sheep. Applied Animal D, 2013. Sustainability in Aquaculture: spectives on Sentience, Pain, Fear and and Haddock (Melanogrammus Aeglefi- Avoidance in Goldfish (Carassius auratus). Behaviour Science, vol. 148, pp.28–36. Present Problems and Sustainable Solu- Stress. Applied Animal Behaviour Science, nus) Caught by Trawl: Fish Behaviour, Applied Animal Behaviour Science, vol. tions. Ocean Yearbook 27, edited by vol. 86, pp. 225-50. [37] Mendl M, et al, 2010. Dogs Showing Stress and Fillet Quality. Fisheries Research, 113, pp. 247-54. A. Chircop, S. Coffen-Smout and A. Mc- Separation-Related Behaviour Exhibit a vol.189, pp. 42–54. [13] Yue S, Moccia R D, and Duncan I J H, Connell, Martinus Nijhoff Publishers, pp. [25] Dunlop R, Millsopp S, and Laming P, ‘Pessimistic’ Cognitive Bias. Current Biolo- 2004. Investigating Fear in Domestic Rain- 291–322. www.brill.com/ocean-year- 2006. Avoidance Learning in Goldfish gy, vol. 20, pp. R839-40. bow Trout, Oncorhynchus mykiss, Using an book-27

16 I FROM THE RESEARCH I 17 FROM THE RESEARCH

– Have some degree of awareness. Thus ed vigilance is termed direct reciprocity Intraspecific variation in behavioural phe- set up cleaning stations on reefs where a predator and expecting they will return. Sentience fishes should have some form of cons- and was thought to exist only in birds notype, often termed the bold and shy client fish, often predatory, arrive and are Pinto et al. [11] observed the number of in fishes ciousness such that they can differentiate and mammals. The benefits of engaging continuum, affects decision making in a cleaned of parasites [11]. If the service is client bites when cleaner wrasse were un- and recognise themselves as distinct from in this behaviour are obvious; rabbitfish consistent manner in many fish species. good then the clients will return and the observed or observed by a potential client Lynne U. Sneddon (Dr.) others. pairs have increased foraging success by For example, rainbow trout (Oncorhynchus cleaner wrasse gets repeat business. The and found that bites were dramatically penetrating deeper into the coral crevices mykiss) display disparate personalities parasites are nutritious but the client’s skin reduced when a client was watching. Recent empirical evidence has shown University of Liverpool, and reduced predation. This is an excellent where active, aggressive dominant individ- and mucus are more so. Therefore, some- These results demonstrate the cleaner is that fishes do indeed have some ability School of Biological Sciences, example of a complex relationship within uals take risks and are classified as bold. In times the cleaner wrasse will nibble the cli- aware of being watched and that its own within each criterion which shall be re- The BioScience Building, species but what about between species? contrast shy trout are risk averse, less active ent. This is a risky strategy when cleaning behaviour will have an impact upon the viewed below. Quoting Redouan Bshary Liverpool L69 7ZB, and submissive [8] [9]. In some opinions ‘Behaviourally speaking, fish can do any- It has been well documented that giant United Kingdom, fish were believed to be automatons only thing a mammal can do’ [1]. Yet we treat moray eels (Gymnothorax javanicus) and [email protected] capable of reflexive behaviours (e. g. [10]) fish quite differently to mammals which is grouper fish(Epinephelidae) form a coop- but numerous studies on personality and curious? erative hunting partnership [1]. These asso- Introduction risk taking in fish including rainbow trout ciations are non-random since individuals Fishes are used in a variety of contexts and demonstrate that these individual charac- Forming relationships choose specific partners so must remember in incredibly large numbers. Trillions of fish teristics influence decision making and thus these individuals. The groupers use sig- are caught or farmed each year to pro- Fishes are capable of having complicated each fish assesses risk in a different way. nals to initiate joint searching and show vide foodstuff for humans or other animals. relationships both intra- and inter-specifi- Assessment of risk can also be influenced moray eels to prey hiding places so they Millions are employed as models for exper- cally. For example, coral reef rabbitfishes by external factors and behaviour altered can chase them out from small crevices imental studies. Fishes are also used for rec- (Siganus) form pairs where they use subtle accordingly. Cleaner wrasses (Labridae) which the bulkier grouper cannot. This reational purposes in sport or as a hobby. communication signals to perfectly match signalling is dependent on how hungry Numerous species are held in public their partner’s behaviour [2]. Whilst one the grouper is but both partners benefit aquaria and fishes are the most numerous fish forages in the coral crevices of their from the association foraging at a greater pet held in home aquaria or ponds. Recent environment, the other fish remains vigilant rate together than when alone. These two empirical studies have demonstrated the looking out for predators (Fig. 1). They reg- species use their complementary hunting capacity for pain and sentience in fishes ularly change roles and this matching of skills to enable them to catch more prey which may lead to suffering. This review behaviour requires the ability to understand fish. Again the use of a signalling system presents the evidence and biology of pain the intentions of each other. This coordinat- demonstrates that the two species can com- and sentience in fishes that make a com- municate and decipher intent and embark pelling case for the capacity to experience on a joint venture together to the benefit of negative affective states. From the neuro- both individuals. anatomy of the nervous system, physiologi- cal responses and through to whole animal Cognitive ability behavioural changes, pain is highly con- served and comparable with mammals. To dispel the myth that fishes, goldfish in This has important implications for how we particular, have a three second memory a treat fish which suggests a more ethical and plethora of studies have investigated the humane management should be adopted. cognitive ability of fishes and not found it lacking. Goldfish(Carassius auratus) can Defining Sentience navigate mazes and can remember the location of spatial cues to reach a target According to Broom’s definition [7]a sen- area [3]. Furthermore, this species has a Figure 3: (A) Section of the maxillary branch of the trigeminal nerve tient being has some ability to: concept of time and learned to press a lever of rainbow trout showing the presence of A-delta and C fibres (×1000, scale bar=2 μm; [20]). (B) Responses of trigeminal recep- – Evaluate the actions of others in relation at a specific time of day to get a reward tors on the head of rainbow trout. Recordings show responses to itself and third parties. I would inter- in an operant learning paradigm [4]. Af- Figure 1: Direct reciprocity is rarely seen to heat, cold, chemical (1% acetic acid applied topically) and pret this as being able to form relation- in birds and mammals but here are photo- ter training, guppies have been shown to mechanical stimuli. For each recording, upper trace indicates stimu- ships within and between species. graphs depicting this complex behaviour in possess numerical skills and can recognise lus applied to the skin, middle plots instantaneous firing frequency the number of dots on test cards always – Remember some if its own actions. Here rabbitfishes. The foraging individual (in the (IFF, calculated from intervals between successive action potentials), choosing the larger number no matter the fishes should have the cognitive ability to head-down position) feeds in cracks and and bottom shows extracellular, single unit recording from the trige- crevices in the substratum, while the vigilant size, distribution or combination of dots [5] minal ganglion. This example is from a polymodal nociceptor show- learn and remember past experiences. individual is positioned in the water column (Fig. 2). These are just a small number of ex- ing slowly adapting responses to heat, chemical and mechanical – Assess risks and benefits. Thus fishes with its head up. Note the obstructions to amples demonstrating how well developed stimulation but not to cold stimulation [19]. (C) Mean time (+S.E.) must be able to assess the pros and cons the visual field of the forager, suggesting fishes’ cognitive ability is review( in [6]). Figure 2: (A) Test apparatus for the abstract numerical discrimination taken for the treatment groups to begin ingesting food (n=5 rainbow of a situation and make decisions based high vulnerability to predation and the unobs- test. Subjects were required to choose the stimulus with the greatest trout per group). There was a significant difference in the time taken upon this assessment. tructed field of perception of the vigilant fish. Decision making number of orange dots. (B) Stimuli used in numerical discrimination to resume feeding between the groups (F4,20=7.29, P=0.003; (a) Siganus corallinus, (b) S. vulpinus, training consisted in two groups of dots differing in numerosity. [27]). (All figures reproduced by kind permission of Elsevier.) – Have some feelings. The ability to ex- (c) S. doliatus, (d) S. puellus. (Taken from [2], Being able to assess the risks and benefits Here, we depicted two examples of 3 vs. 4 contrast, with cumulative perience positive and negative affective photographs taken and owned by Jordan of a situation and then make a decision surface area controlled (I) and not controlled for (II). states and be influenced by the state of M. Casey, reproduced under a Creative based upon that assessment indicates sen- (Taken from [5] under the terms of the Creative Commons Attribution others. Commons License CC BY [2].) tience since this involves reasoning [7]. License CC BY).

18 I FROM THE RESEARCH I 19 FROM THE RESEARCH

potential new client. Thus, it does not bite reacting to a predator cue performed an Conclusion Recreational fishing involves capture of fish References Take Home Message its client and assesses the risk and benefits increase in freezing behaviour even though This review provides compelling evidence for food or in the practice of catch and re- [1] Bshary R, Hohner A, Ait-el-Djoudi K, of this behavioural strategy and how it may they were not exposed to the predator cue that fishes meet the criteria for animal lease. and Fricke H, 2006. Interspecific commu- Recent research shows that at least influence another individual. [18]. Thus the fear response in the exposed sentience where they possess some abili- nicative and coordinated hunting between Catching and killing fish quickly and hu- some, if not all, fish species are sen- fish was recognised by the observer fish ty to form relationships, possess complex groupers and giant moray eels in the Red manely [25] thereby treating them in a tient. They can form relationships Positive and negative and the observer exhibited a similar an- learning and memory abilities, can make Sea. PLoS Biol. 4 (12): e431. humane manner means any suffering is with conspecifics or with individuals affective state ti-predator response even when there was decisions based on risks and benefits, can reduced. However, the practice of catch of other species, can solve complex [2] Brandl S J & Bellwood D R, 2015. Co- Studies have sought to understand the na- no cue to signal danger demonstrating experience positive and negative affective and release does involve releasing fish learning and memory tasks and make ordinated vigilance provides evidence for ture of positive and negative ‘feelings’ in emotional contagion. states including being affected by the affec- with hooking injuries after what may be a decisions based on the assessment of direct reciprocity in coral reef fishes. Sci- fishes. Surgeon fishAcanthuridae) ( when tive state of others, and show self-aware- stressful event. Therefore, welfare improve- risks and benefits, are able to expe- entific Reports ,5 Article number: 14556 exposed to a moving model of a cleaner Self-awareness and ness. Only a few examples are given here ments should be investigated to ensure rience positive and negative affective wrasse with brushes voluntarily swim par- consciousness but there are many more including tool [3] López J, Broglio C, and Rodríguez F, the released fish have the best chance of states, show self-confidence, use tools allel to the model and receive what could Can fish recognise themselves as distinct use and building of complicated structures 1 et al, 1999. Multiple spatial learning survival. Finally, fishes are also used as a and are able to build complicated be called a massage [12]. They do not en- from other individuals? Are they self-aware (review in [6]). strate-gies in goldfish (Carassius auratus). companion animal and are probably the structures. gage in this behaviour if the model cleaner and do they show some degree of con- Anim Cognition 2, 109–120. If fishes are sentient then this has implica- most numerous pet with large numbers kept wrasse is stationary. Those surgeon fish that sciousness? A study [21] clearly demon- Fish are by far the most widely used tions for the way we treat them. In animal in home aquaria and ponds [26]. Thus leg- [4] Gee P, Stephenson D, and Wright D E, engaged with the model had lower circu- strated cichlid fish can recognise their animals. For human consumption, experimentation juvenile and adult fishes islation and protection should be reviewed 1994. Temporal discrimination learning lating cortisol levels compared to individu- own odour and distinguish it from others several trillion fish are obtained an- are protected by legislation and regulations to improve and maintain high welfare of operant feeding in goldfish. Journal of als that did not have a massage and the in a choice test. Mirror self-recognition tests nually from aquaculture or fisheries. in Europe (EC Directive 2010/63). Given standards in the ornamental fish industry. the Experimental Analysis of Behavior 62, researchers concluded this had a calming, were recently thought to be the gold stand- Millions of fish are used for animal fish are now the second most popular ex- 1–13. positive effect on the fish. Therefore, this ard of proving consciousness if an animal To conclude it is not only in the fish’s inter- experiments, and fish are proba- perimental across Europe it is vital we treat can be considered as an example of pos- could recognise itself in a mirror [7]. When est to treat them ethically but it is also in bly the most commonly kept pets. In [5] Dadda M, Agrillo C, Bisazza A, and experimental fish in a humane and ethical itive affective state in fish. There has been presented with a mirror, Manta rays (Mabu- our best interests that fish are healthy and view of this large number of animals Brown C, 2015. Laterality enhances nu- manner. This not only ensures they remain a focus on negative affective states in fish la) perform self-directed behaviours waving in a good state if we are to use them as involved, questions about improving merical skills in the guppy, Poecilia retic- healthy but will also lead to more robust since most legislation suggests the ability to at the mirror and blowing bubbles [22]. research models, as foodstuff, as a pet or animal welfare in fish are even more ulata. Front. Behavioral Neuroscience 9. data and valid scientific outcomes. Fishes suffer is the main driver behind protecting a Cleaner wrasse pass the mirror self-recog- if we wish to maintain sustainable popula- important. A considerate handling doi: 10.3389/fnbeh.2015.00285 are used as an important source of protein. particular species. nition test with flying colours. Indeed when tions for fishing. of fish not only improves their wel- Large scale fisheries catch vast numbers of [6] Brown C, 2015. Fish intelligence, sen- a coloured dot was put on the wrasse and fare, but also the benefit for humans. Current scientific evidence proves that fish fishes and improving their welfare during tience and ethics. Animal Cognition 18, they saw themselves in a mirror they sought A more careful catch increases the possess nociceptors, receptors that prefer- the capture and slaughter process would 1-–17. to rub off the dot by rubbing that part of food safety of the fish meat, a more entially detect painful, damaging stimuli; enhance food security. The Farm Animal the body on the substrate [23] (Fig. 4); this species-appropriate farming increas- [7] Broom D, 2014. Sentience and Animal adverse physiological and behavioural Welfare Council (FAWC, UK) have stated behaviour has only been recorded in birds es the product quality as well as the Welfare. CABI: Oxfordshire, pp 185. responses to painful treatment that are pre- that fish should be treated in farming and and mammals previously and is considered profitability of the farm. Existing ani- vented when pain-killing drugs are admin- aquaculture humanely since they experi- [8] Sneddon L U, 2003. The bold and the evidence of consciousness. Thus there is mal welfare legislation should be re- istered; and that when experiencing pain ence pain [24]. Improving welfare means shy: speed of learning in rainbow trout. evidence in some species of fish for the ca- viewed to determine what measures fishes do not show appropriate fear or an- fish are healthy and that could improve J. Fish Biol. 62, 971–975. pacity for self-recognition and awareness. are needed to improve fish welfare ti-predator behaviour (reviews in [13] [14] economical return for the farming industry. [9] Thomson J S, Watts P C, Pottinger T G, [15] [16]; Fig. 3). Therefore, there is am- and keep it on a high level. (Ed.) and Sneddon L U, 2011. Physiological and ple evidence of pain in fish. Furthermore, genetic correlates of boldness: characteris- the responses to pain are not reflexive and ing the mechanisms of behavioural varia- are influenced by the presence of others. In tion in rainbow trout, Oncorhynchus my- zebrafish (Danio rerio), individuals subject kiss. Horm. Behav. 59, 67–74. to fin clipping where a portion of tail fin is removed for genotyping, recovered more [10] Rose J D, 2002. The neurobehavioral quickly in a group compared with isolated nature of fishes and the question of aware- and paired zebrafish [17]. This phenom- ness and pain. Rev. Fisher. Sci. 10, 1–38. enon is termed social buffering where the [11] Pinto A, Oates J, Grutter A, and social environment can modulate affective Bshary R, 2011. Cleaner wrasses state, thus, in a familiar group of conspe- Labroides dimidiatus are more cooperative cifics the individual may be less affected in the presence of an audience. Curr. Biol. by a negative welfare state. Emotional 21, 1140–1144. contagion, where an observer mirrors the behaviour of an affected individual, has [12] Soares M C, Oliveira R F, Ros A F H, also been investigated in fishes [18]. This Grutter A S, and Bshary R, 2011. Tactile stim- is linked to empathy where humans show ulation lowers stress in fish. Nature Comms. 2, 534. sympathy and human affective state is in- Figure 4: Schematic sequence of posturing, throat-scraping behaviour, and then posturing fluenced by the mental state of another thus again in positions that reflect the throat when a coloured dot is present on cleaner wrasse the emotion is contagious. In zebrafish, presented with a mirror (from [23], reproduced under the terms of the Creative Commons 1 individuals who observed conspecifics Attribution License CC BY). Catch and release is prohibited in Germany, Austria and Switzerland because catching fish for purposes other than food is not a legally permissible reasonable cause to inflict pain and suffering on them. (Ed.)

20 I FROM THE RESEARCH I 21 FROM THE RESEARCH FROM THE RESEARCH

[13] Sneddon L U, Elwood R W, Adamo [25] Cooke S J and Sneddon L U, 2007. and under what circumstances they might Other promising lines of research include S, and Leach M C, 2014. Defining and as- Animal welfare perspectives on recrea- Fishes are smart and feel have them. preferential attachment (aka friendships) in sessing pain in animals. Anim. Behav. 97, tional angling. Appl. Anim. Behav. Sci. guppies [21], social motivation in cichlids pain: What about joy?* Several decades ago, the positive psychol- 201–212. 104, 176–198 [22], and free-choice exploration in zebraf- ogy movement sought to correct a similar 1 ish [23]. Most recently, research with ze- [14] Sneddon L U, 2015. Pain in aquatic [26] Sneddon L U and Wolfenden D C C, Becca Franks (Dr.), bias in the human literature, arguing that 1 brafish suggests that when they are housed animals. J. Exp. Biol. 218, 967–976. 2019. Ornamental Fish (Actinopterygii). Jeff Sebo (Dr.), beyond being a luxury, positive psycholo- 2 in naturalistic environments, they engage in In: UFAW Companion Animal Handbook, Alexandra Horowitz (Dr.) gy is at the very core of human experience [15] Sneddon L U, 2018. Comparative heightened shoaling behaviour — protract- (Ed. J . Yeates). Wiley Blackwell, pp. 440– 1  [8]. More recently, the field of animal wel- physiology of nociception and pain. Department of Environmental Studies, ed bouts of tight group cohesion and in- 466. fare also began to consider ways to pro- Physiology 33, 63–73. New York University, creased behavioural synchrony — another mote positive welfare beyond simply trying [27] Sneddon L U, 2003. The evidence for 285 Mercer Street, 8th floor, behaviour that may yield insights for future [16] Sneddon L U, 2019. Evolution of noci- to alleviate poor welfare [9] [10] [11]. pain perception in fish: the use of morphine New York, NY 10003, USA work on positive emotion in fish [23]. Fur- ception and pain: Evidence from fish Even though fish have yet to benefit directly as an analgesic. Appl. Anim. Behav. Sci., [email protected] ther developing operational definitions of models. Phil. Trans. Roy. Soc. Lond. B, from these correctives, both fields – positive 83, 153 –162. 2  positive emotions such as joy, gratitude, 374, 20190290. Department of Psychology, psychology and animal welfare – contain and serenity will allow us to test whether Barnard College, Columbia University, insights about ways forward for research [17] White L J, Thomson J S, Pounder K C, such terms should continue to be reserved 3009 Broadway, New York, on fish pleasure. Coleman R C, and Sneddon L U, 2017. NY 10027, USA to a single species (i. e., ourselves). The impact of social context on behavior In positive psychology, Fredrickson [12] The human impact on fish is increasing at and the recovery from welfare challenges Sneddon et al. [1] write that “more fund- has identified ten core positive emotions: an alarming rate: aquaculture and the use in zebrafish, Danio rerio. Anim Behav. ing is needed in the area of fish welfare joy, gratitude, serenity, interest, hope, of fish in science is expanding rapidly, as to provide robust empirical evidence we pride, amusement, inspiration, awe, and [18] Fernandes Silva P, Garcia de Leaniz are habitat degradation and threats to wild can use to inform the humane and ethical love. While these might seem like strange C, and Luchiari A C, 2019. Fear contagion populations from overfishing. The pressures treatment of fish.” We ask: What sort of words to apply to a fish (at least from a be- in zebrafish: a behaviour affected by famili- to understand fish sentience are more ur- additional empirical evidence is required? haviourist perspective), the field of animal arity. Animal Behaviour 153, 95–103. gent than ever, yet both academics and the welfare is beginning to develop methodol- Thus far, the debate over fish sentience has general public remain focused primarily on [19] Ashley P J, Sneddon L U, and ogies for identifying similar experiences in focused almost entirely on whether fish can pain, where the evidence is already com- McCrohan C R, 2007. Nociception in fish: nonhuman animals. For example, studies feel pain (e. g., [2]). Pain is a complicated pelling. We need a more complete picture stimulus–response properties of receptors on cognitive biases in nonhuman animals concept that cannot be proven or disprov- of fish sentience. To ground decision-mak- on the head of trout Oncorhynchus mykiss. (Peter Singer) suggest that animals with en in a species through a single, stand- ing about humane and ethical treatment, Brain Res. 1166, 47-54. better welfare have more optimistic inter- alone experiment [3]. The body of evi- the biggest need going forward is for re- pretations of ambiguous cues [13] [14]. In [20] Sneddon L U, 2002. Anatomical dence as a whole provides strong reason search on positive emotional experience in other words, they are hopeful. In addition, and electrophysiological analysis of the to accept that fish have experiences that fish, including joy. behavioural research with many species trigeminal nerve of the rainbow trout, we can plausibly describe as pain: fish has provided evidence of curiosity (e.g., Onchorynchus mykiss. Neurosci. Letts., pay to avoid potentially painful stimuli, for- [15] [16] [17]), which is defined as the 312, 167–171. feit good outcomes for the sake of avoiding Take Home Message such stimuli, and seek out analgesics after motivation to gain information. In other [21] Thünken T, Waltschyk N, Bakker potentially painful procedures [4]. These words, they display interest. The evidence for fishes feeling pain T, and Kullmann H, 2009. Olfactory behaviours require active decision making The existing literature on fish pleasure is is now so strong and comprehensive self-recognition in a cichlid fish. Animal and are thus easier to explain by accepting slim, but promising. Studies dating back to that arguments against it are increas- Cognition 12, 717–724. that fish can experience pain rather than the early twentieth century have examined ingly difficult to defend in a balanced [22] Ari C and D’Agostino D P, 2016. assuming that they cannot. spontaneous leaping and somersaulting academic discourse. But there is more Contingency checking and self-directed to empathy than just pain. Recent re- Pain, however, is not the sum-total of sen- behaviour in fish, as well as voluntary and behaviors in giant manta rays: Do elasmo- search suggests that fishes have an tience. Sentience is a complicated concept, nonfunctional object manipulation and so- branchs have self-awareness? Journal of impressive range of cognitive abili- but most scholars agree that it involves the cial interaction that fulfill the criteria of play Ethology 34, 167–174. ties, including the ability to feel pos- ability to experience pain and pleasure [5] [18] [19]. As a naturally occurring behav- itive emotions in the form of play and [6]. While scientific studies over the past iour, play may provide the best example of [23] Kohda M, Hotta T, Takeyama T, other behaviours that are likely to in- several years have indicated that fish have a behaviour that is widely observed across Awata S, Tanaka H, Asai J Y, et al, 2019. volve a positively valued experience. the cognitive equipment necessary for rich the animal kingdom [20]. And, in humans If a fish can pass the mark test, what Having made the argument for pain, mental lives [7], the scientific study of fish at least, play is associated with intensely are the implications for consciousness research can now focus on other as- pleasure has been relatively neglected. positive emotional experiences like joy and and self-awareness testing in animals? pects of fish sentience. This will not Thus, focusing future research on fish pleas- amusement. Studies of participation in play PLoS Biol. 17, e3000021. https://doi. only provide a more complete picture ure is likely to generate a wealth of theo- may be the most fruitful way to develop the- org/10.1371/journal.pbio.3000021 of fishes’ mental life and abilities, but retically and practically useful information, oretical and empirical markers of positive [24] FAWC, 2014. Opinion on the welfare also promote their well-being and including answers to questions about what emotional experiences in nonhuman ani- of farmed fish at the time of killing.https:// protection. (Ed.) kinds of positive experiences fish may have mals, including fish. www.gov.uk/government/publications/ fawc-advice-on-farmed-fish-welfare * First published in: Animal Sentience (2018): Franks et al. on Sneddon et al. on Sentience Denial. Translated by Billo Heinzpeter Studer. Courtesy of the publisher and authors.

22 I FROM THE RESEARCH I 23 FROM THE RESEARCH

References [14] Harding E J, Paul E S, and Mendl M T, an attempt to keep or re-establish the bal- Nowadays, the concept of quality of life has [1] Sneddon L U, Lopez-Luna J, Wolfend- 2004. Animal behaviour: Cognitive bias Farming fish: ance. Stimuli are received by a multitude been increasingly adapted to animals [11]. en D C C, Leach M C, Valentim A M, and affective state. Nature, 427(6972), from stress to quality of possible receptors linked to different Owners, farmers, caretakers or veterinarians Steenbergen P J, Bardine N, Currie A D, 312. of life and to the dish sensory organs (e. g. eyes, skin). This infor- complete questionnaires on objective (quan- mation is than passed to the brain via the titative) and subjective (qualitative) measures. Broom D M, and Brown C, 2018. Fish [15] Berlyne D E, 1966. Curiosity and ex- peripheral nervous system. Once there, the Qualitative measures rely on the perceived sentience denial: Muddying the waters. ploration. Science, 153(3731), 25–33. Leonor Galhardo (Dr.) Animal Sentience 21(1). stimuli activate many relevant brain areas, mental state, personality and reactions of [16] Glickman & Sroges, 1966 Instituto Superior which will organise, prioritise and label the animals and have been validated against [2] Key B, 2016. Why fish do not feel de Psicologia Aplicada (ISPA), received information in what is called the well-known physiological and behavioural [17] Hall B A, Melfi V, Burns A, McGill D M, pain. Animal Sentience 3(1). Lisbon, Portugal, animals’ cognitive assessment (also named measures. Quality of life evaluations dif- and Doyle R E, 2018. Curious creatures: [email protected] ‘appraisal’). The appraisal process includes fer from more classical on-farm evaluation [3] Sneddon L U, Elwood R W, Adamo A multi-taxa investigation of responses cognitive and emotional components. It schemes because the latter use quantitative, S A, and Leach M C, 2014. Defining and to novelty in a zoo environment. PeerJ, 6, 1. Introduction categorises information according to pre- as opposed to qualitative, animal-based assessing animal pain. Animal Behaviour, e4454. 97, 201–212. Animal welfare has been defined in different vious experiences and acquired memories, parameters, and also because they include [18] Burghardt G M, 2005. The origins of ways according to the emphasis the authors including those related to emotions such as resource-based parameters. [4] Sneddon L U, 2015. Pain in aquatic vertebrate play: Fish that leap, juggle, and give to different aspects of the concept. learned fear, pain or comfort, and also se- animals. Journal of Experimental Biology, tease. In The Genesis of Animal Play: Testing Many definitions have been proposed, but a lects the most appropriate coping response 2. Assessing fish welfare 218(7), 967–976. the Limits (p. 501). Cambridge, MA: MIT classical one, by Broom [1] captures the es- [7]. This is the reason why the more the Indicators of welfare are the responses of [5] Broom D M, 2016. Sentience and ani- Press. sence of what animal welfare encompasses, perceived stimulus is under the fish's own animals while dealing with their baseline expectations, understanding and control, mal welfare: New thoughts and controver- [19] Fagen R, 2017. Salmonid jumping remaining updated and operational. Broom or changing environment. Operational indi- the less stressful it is appraised. sies. Animal Sentience 5(11). and playing: Potential cultural and welfare defined animal welfare as the individual cators of welfare should be science-based, state with regard to its attempt to cope with able to assess long-term welfare, measura- [6] Harnad S, 2016. Animal sentience: The implications. Animals, 7(6), 42. The physiological and behavioural re- its environment. The individual state includes ble in aquaculture settings and relevant to other-minds problem. Animal Sentience 1(1). [20] Ahloy-Dallaire J, Espinosa J, and Ma- sponses to stress are meant to be adaptive, a physical and a mental dimension, which even if they transiently decrease welfare. husbandry practices [12]. [7] Brown C, 2015. son G, 2017. Play and optimal welfare: Fish intelligence, sentien- are inextricably related. Whether the stimulus is negatively or posi- Does play indicate the presence of positive The physiological stress response ranges ce and ethics. Animal Cognition, 1–17. tively appraised, it induces a physiological affective states? Behavioural Processes. Measures of organic functioning in fish from immediate and reversible neuroen- [8] Seligman M E P and Csikszentmihalyi have been developed for many years now. response with the release of both adren- docrine changes to prolonged chemical M, 2000. Positive psychology – An intro- [21] Heathcote R J P, Darden S K, Franks But studies of their mental state have been aline and cortisol (in fish) aiming to pre- alterations. Components of this response duction. American Psychologist, 55(1), D W, Ramnarine I W, and Croft D P, 2017. more difficult not only due to its subjectivity pare the body for action. Negative stimuli have been used as measures of welfare. 5–14. Fear of predation drives stable and differen- but also because there is no direct way to may trigger a vast array of self-protective Among these, cortisol has been widely tiated social relationships in guppies. Scien- responses in fish, from the classical fight- [9] Boissy A, Manteuffel G, Jensen M B, access this information. Still, many indirect used as a stress hormone, in the sense tific Reports, 7, 41679. or-flight response to very complex and Moe R O, Spruijt B, Keeling L J, Winck- approaches have been explored for some of negative contexts and diminished wel- highly contextual behaviour [8] [9]. Posi- ler C, Forkman B, Dimitrovi I, Langbein J, [22] Galhardo L, Almeida O, and Oliveira species. Broom’s concept of welfare rang- fare [13]. Cortisol can be sampled from es from very poor, when animals fail or tive stimuli may produce approach to stim- blood, urine, the body's homogenates or Bakken M, Veissier I, and Aubert A, 2007. R F, 2011. Measuring motivation in a cichlid find permanent difficulties to cope, to very ulus, consumption, or more complex and from the holding water, according to the Assessment of positive emotions in animals fish: An adaptation of the push-door para- good, when they enjoy good health and specialized patterns of behaviour. Apart species and the specific research context to improve their welfare. Physiology & digm. Applied Animal Behaviour Science, are able to express much of their potential from levels of the stimuli intensity, duration, and objective. Cortisol is a very impor- Behavior, 92(3), 375–397. 130(1–2), 60–70. as individuals [2]. Appropriate husbandry etc., these responses may become mala- tant metabolic hormone since it powerfully [23] Graham C, von Keyserlingk M A G, [10] Mellor D J, 2014. Positive animal requirements are relevant for welfare but, as daptive and cause prolonged poor mental affects physiology, behaviour and brain and Franks B, 2018. Free-choice ex- welfare states and encouraging environ- the World Organisation for Animal Health and physical states. In fish, states of chron- functions. However, various studies in verte- ploration increases affiliative behaviour ment-focused and animal-to-animal interac- (OIE) highlights in its definition [3], welfare ic stress dramatically threaten the immune brate species, including fishes, have report- in zebrafish.Applied Animal Behaviour tive behaviours. New Zealand Veterinary is about the internal state of animals and, to system, creating pathological conditions, ed increased cortisol levels in contexts of Science, 203, 103–110. Journal, 63(1), 9-16. understand it, validated physiological and which are very difficult to revert [10]. environmental enrichment and/or positive [11] Yeates J W and Main D C J, 2008. [24] Franks B, Graham C, and von Key- behavioural measures must be used. Quality of life has been defined as a stable excitement, showing that cortisol is better serlingk M, 2018. Is heightened-shoaling interpreted as a measure of arousal [14] Assessment of positive welfare: A review. All views of welfare are impregnated with and prolonged state of well-being. Origi- a good candidate for positive emotional [15]. Understanding its dynamics imply The Veterinary Journal, 175(3), 293–300. moral values. The FishEthoBase mentions the nally, meant to apply to humans, quality of behavior in zebrafish?Animals , 8(9), 152. life is related to the subjective and dynamic taking into consideration related variables [12] Fredrickson B L, 2013. Positive emo- potential of the species and individuality [4]; self-evaluation of the individual’s circumstanc- such as species-specific baseline levels and tions broaden and build. In P. Devine & A. the Swiss Animal Welfare Act includes philo- es and the extent to which these meet its patterns of diurnal variation. Plant (Eds.), Advances in experimental so- sophical concepts, such as dignity or intrinsic expectations, which results in feeling-relat- cial psychology (Vol. 47, pp. 1–54). San value [5]. Whatever the approach, animal Other physiological indicators of stress used, ed (affective) responses. The measurement Diego, CA: Academic Press. welfare needs to be understood in the scope some of which post-mortem, include blood of the animals’ natural adaptations and their of quality of life led to the development of metabolites (e. g. glucose, lactate, hepatic [13] Baciadonna L and McElligott A, physical and mental coping mechanisms to multi-dimensional evaluation indexes with glycogen, heatshock proteins and meta- 2015. The use of judgement bias to assess go about their life [6]. application in multiple onsets. These are bolically active enzymes), immune system welfare in farm livestock. Animal Welfare, quantifiable measurements related to differ- function (e. g. number of circulating lympho- Any time a fish faces a stimulus, which 24(1), 81–91. ent dimensions of welfare in humans (e. g. cytes), other hormones and neurotransmit- can potentially disrupt its internal balance pain, disease, stress) and use behavioural, ters, corticosteroid-receptors abundance and (stressor), a stress response is triggered in physiological and biochemical markers. specific gene regulatory pathways [2].

24 I FROM THE RESEARCH I 25 FROM THE RESEARCH

In aquaculture contexts, measures of health foraging and feeding behaviour, ventilatory clude subaquatic cameras, remotely operated reduce the stress impact of transport. and productivity are often used as welfare activity, swimming patterns, use of available vehicles, telemetry (e.g. SmartTags), etc. Another study [21] found a reduced cor- indicators. Physical condition (e. g. spinal area, aggression and its consequences (e. g. Modern monitoring systems allow identify- tisol response to confinement due to pre- deformities, fin erosion, injuries), growth injuries). In turn, mental states started to be ing behavioural indicators at individual and vious training to make this event predic- and reproductive rates, incidence of dis- scrutinized later and have been inferred group-level in big tanks, with great advan- table through visual signalling (Figure 1). ease and mortality levels are usual exam- from studies of preferences and operant tages for high standard husbandry routines. A third study [22] also found that neopho- ples [16] [17]. However, all of them are behaviour, anticipatory activity (reward an- bia (aversion to novel objects) decreases in late indicators of the internal state and pro- ticipation), stereotypes and other abnormal 3. From stress to quality of life animals housed with familiar conspecifics vide little or no information on early mental behavioural patterns, exploratory and play In aquaculture, it is impossible to avoid (Figure 2). disturbances. Whether the objective is to behaviour, and cognitive bias (inference of procedures such as grade, harvest trans- Giving animals a degree of control over reduce stress or to promote good levels of optimism/pessimism). Whether these behav- port, slaughter, among many others, which their environment, where animals access re- welfare, these measures portray a state that ioural categories reflect negative or positive cause disturbance, fear and, sometimes, sources or act on their own initiative rather can already be very difficult and expensive mental states is not linear. Still, approach major stress. A high profile husbandry than in response to external stimuli, has been to revert. As such, they are of little practical behaviour, behavioural diversity and explo- should aim at only minimising stress but related to a significant welfare increase in use for a well-refined husbandry practice. ration/play are usually related to positive also at promoting opportunities for the an- many species. For example, in aquaculture Earlier and sensitive indicators of stress appraisals; whereas escape behaviour, ste- imals to experience a good quality of life. the potential benefits of self-feeders, opera- have been increasingly preferred because reotypes and other abnormal behavioural ted by individual fish, were related to the interventions in minimising stress can be put patterns are used as measures of negative Best stress management can be achieved selection of diets according to individual into practice at earlier stages. Behaviour appraisals. by reducing unnecessary stressful proce- specific requirements[23] . Control over the is the earliest and subtlest indicator of wel- dures (e.g. some handling and transport), One of the relevant effects of chronic stress environment has also to do with providing fare. Its evaluation is practical, cheap and by following the available species-specific is cognitive impairment [19]. Therefore in- significant environmental choices to animals non-invasive, though it is often difficult to best practices and by taking into conside- dicators related to cognitive abilities have Figure 2: (e.g. different ranges of temperature or wa- understand and interpret. ration the mental dimension of animals. been studied and could be developed in It is possible to reduce the impact of ine- A. Novel Object (NO) Test in Mozambique tilapia: a table tennis ball filled with sand ter depth, possibility to be or not in social Behaviour is shaped by a number of indi- aquaculture settings (e. g. performance of vitable stressful procedures by taking into placed in the focal male tank, after which trials started. Behaviour of focal males was com- contact with others, to seek shelter, etc.). For vidual (e. g. anatomy, early experiences, specific behaviour, tool use according to consideration fish perceptions (appraisal) pared among three different social contexts: isolated males, in visual contact with a familiar example, a study [24] found that the mere motivation) and environmental characteris- natural behaviour, changes in memory/ and adjusting management procedures companion and in visual contact with an unfamiliar companion. (Photo: © L. Galhardo) provision of a shelter, where juvenile salmons tics, not only related to the present moment learning function). accordingly. For example, a study [20] B. Time spent freezing and exploring the NO in the three social contexts; different letters stay in the vicinity rather than actually using but also shaped throughout the individual represent significant statistical differences between treatments. (Originally published in [22]). it, is enough to reduce their maintenance Methods of monitoring behaviour in aquacul- observed that food conditioned Chinook life of the animal as well as the evolution metabolism. Another study [14] reports that ture tanks have been developed, which in- salmon (Oncorhynchus tshawytscha) would of the species. Understanding these char- Mozambique tilapia (Oreochromis mossam- acteristics is important when considering bicus) males are willing to work through a aspects of welfare. In fact, in relation to push-door to have access to a new tank the individual coping style, the lack of compartment for food or social partner con- activity in a shy animal (passive coping, tact (Figure 3). high cortisol responder) cannot be inter- Therefore, promoting quality of life can be preted as they would be in a bold animal achieved by providing opportunities for op- (active coping, low cortisol responder). For timal social contexts, encouraging mental example, a study [18] found that two se- stimulation, behavioural diversity and the lected lines of rainbow trout have different expression of natural behaviour. Positive growth rates depending on their respon- affective states can be further strengthened siveness to stress. Bold fish have higher through a dynamic environment, appropriate growth rates, which may be related to their complexity and a certain degree of control. likelihood to win in competition (greater Some relevant topics that must be addressed aggressiveness) or to direct interference of in order to promote quality of life include: cortisol on growth. • Improving the tanks’ design respecting A behavioural pattern often reflects both or- the anatomy and behavioural features of ganic and mental dimensions of welfare. For specific species; example, regardless of the original causes, excessive inactivity may simultaneously be • Providing behavioural opportunities that both a sign of organic dysfunction (e. g. are as similar as possible to the evolving disease, injury) and a sign of disturbed environment of the species (e. g. bottom- mental states (e. g. discomfort, pain, social feeder fishes should be given sinking Figure 3: fear, etc.). But it is the context and the com- Figure 1: pellets); bination of different indicators which will A. Visual sign used to condition Mozambique tilapia to negative and positive predictable A. Tank with a start compartment where a male of Mozambique tilapia was required to push a door of different weights (price) in order to access the resource compartment. Motivation to • Promoting a better quality of the envi- provide the best behavioural interpretation. events (confinement and feeding, respectively). (Photo: © L. Galhardo) push the door was analysed for three conditions in the resource compartment: substrate-only ronment (including water quality but also Measures of behaviour have consistently B. Cortisol response in the baseline (social isolation for 8 days), predictable and (control), substrate + food and substrate + social partner. (Photo: © L. Galhardo) all stimuli that may impact fish percep- been used to assess organic functioning in unpredictable events after (a) confinement and (b) feeding events. B. Latency (s) for opening the push-door as price increases to obtain access to different tion—auditory, visual, chemical, vibra- fish for a long time [12]. Examples include: ** level of statistic significance, P < 0.01. (Originally published in [21]). resources: food, social partner and control (substrate only (Originally published in [14]). tional, etc.);

26 I FROM THE RESEARCH I 27 FROM THE RESEARCH

• Providing appropriate environmental relative to fish neuro-anatomic structures References [12] Martins C I M , Galhardo L, Noble [21] Galhardo L, Vital J, and Oliveira R F, enrichment schedules, for physical and and cognitive abilities allow one to infer Take Home Message C, Damsgård B, Spedicato M T, Zupa W, 2011. The role of predictability in the stress [1] Broom D M, 1986. Indicators of poor cognitive stimulation (e.g. training), in that they must make use of high cognitive Beauchaud M, Kulczykowska E, response of a cichlid fish.Physiology and welfare. British Veterinary Journal, 142, order to promote physical and mental resources and, at least, a certain degree of Data on fish health and growth are Massabuau J-C, Carter T, Planellas S R, Behavior 102: 367–372. 524–526. Bshary R and Brown C, 2014. fitness and well-being; consciousness. still often used in aquaculture as indi- and Kristiansen T, 2012. Behavioural in- Fish cognition. Current Biology: 24, [22] Galhardo L, Vitorino A, and cators of fish welfare. However, such dicators of farmed fish welfare. In:van • Forming appropriate social contexts in So, if fishes are sentient, it is in their interest R947–50. Oliveira R F, 2012. Social familiarity mod- data provide little or no information de Vis, Kiessling, Flik, G, Mackenzie, S. terms of composition, density and stabil- not to suffer and to feel well [30] When ulates personality trait in a cichlid fish. Biol- on early mental disorders, and as late [2] Broom D M, 2014 . Sentience and an- (Eds.), Welfare of farmed Fish in Present ity over time, according to the species- farming them, humans have the moral re- ogy Letters, 8(6), 936–938. indicators of internal condition, they imal welfare. CABI, UK. and Future Production Systems. Springer: specific social features; sponsibility to avoid unnecessary suffering represent a condition that is difficult New York, pp 20–45. [23] Attia J, Millot S, Di-Poï C, Bégout, and to improve their quality of life. Therefore, [3] OIE, 2008. A new definition for the • Providing subordinate animals with and costly to reverse. A far-sighted M L, Noble C, Sanchez-Vazquez F J, measures should be consistently adopted to Terrestrial Animal Health Code: ‘animal [13] Ellis T, Yildiz H Y, López-Olm- means to escape, hide and have access aquaculture management therefore Terova G, Saroglia M, and Damsgård B, integrate this duty in the scope of the aqua- welfare’. Forum. World Organisation for eda J, Spedicato M T, Tort L, Øverli Ø, to relevant resources (e. g. food); prefers earlier and sensitive stress in- 2012. Demand feeding and welfare in culture’s mission and activities. Even when Animal Health. Website accessed on 23 and Martins C I, 2012. Cortisol and finfish dicators to implement early-stage farmed fish. Fish Physiology and Biochemis- • Promoting excellent practices during information is lacking on which ways and April 2020: https://www.oie.int/index. welfare. Fish physiology and biochemistry, stress reduction interventions. The be- try, 38(1), pp.107–118. handling, transport and slaughter. php?id=169&L=0&htmfile=chapitre_aw_ contexts fishes may suffer, adoption of the haviour of fishes is the earliest and 38(1), 163–188. precautionary principle remains the most introduction.htm [24] Millidine K J, Armstrong J D, most subtle indicator of their well- [14] Galhardo L, Almeida O, and 4. For ethical farming and ethical solution for a best practice approach. and Metcalfe N B, 2006. Presence of shel- being. Its assessment is practical, [4] Studer B H, 2015. How does FishEtho- Oliveira R F, 2011. Measuring motivation a better dish ter reduces maintenance metabolism of ju- The ethical aquaculture is a broader con- cost-effective and non-invasive; how- Base define fish welfare?.FishEthoBase Re- in a cichlid fish: an adaptation of the push- The moral status of animals has to do with the venile salmon. Functional Ecology, 20(5), cept, also encompassing that of sustainabil- ever, behaviour is often difficult to un- search Group (editor). FishEthoBase. Web- door paradigm. Applied Animal Behaviour reason humans should be concerned with 839–845. ity. In this enlarged scope, animal welfare derstand and interpret. site accessed in 23 April 2020: http:// Science, 130(1–2), pp.60–70. their protection. In the sphere of moral ethics values have to be balanced against the fishethobase.net/welfare/ [25] Lund V, Mejdell C M, Röcklinsberg H, Behaviour is shaped by a number of [15] von Krogh K, Sørensen C, Nilsson a range of diverse arguments has been the production of good and safe foods, while Anthony R, and Håstein T, 2007. Expand- individual (e. g. anatomy, early expe- [5] Swiss Animal Welfare Act: https:// G E, and Øverli Ø, 2010. Forebrain cell basis for different approaches to the moral preserving wild populations and habitats; ing the moral circle: farmed fish as objects riences, motivation) and environmen- www.fedlex.admin.ch/eli/cc/2008/ proliferation, behavior, and physiology of protection of animals. Nowadays, one of avoiding waste discharge, diseases to of moral concern. Diseases of aquatic orga- tal characteristics, which are not only 414/en zebrafish, Danio rerio, kept in enriched or the most widely accepted of these arguments wild populations and invasion of exotic nisms, 75(2), 109–118. related to the present moment but are barren environments. Physiology & behavior, relies on sentience, or the ability to feel suf- organisms. At the same time, aquaculture [6] Dawkins M S, 2006. A user’s guide to also shaped throughout individual life 101(1), 32–39. [26] Meijboom F L, Bovenkerk B, 2013. fering or pleasure. should not misuse natural resources, should animal welfare science. Trends in Ecology and the evolution of the species. Un- Fish welfare: Challenge for science and promote wealth and fair trade, respecting & Evolution, 21, 77–82. [16] Ellis T, Oidtmann B, St-Hilaire S, The discussion of the moral status of fishes derstanding them is important in or- ethics — Why fish makes the difference. local communities. In this complex but syn- Turnbull J, North B P, MacIntyre C, has been delayed in comparison to that der to be able to draw conclusions [7] Galhardo L, Oliveira R F, 2009. Journal of agricultural and environmental ergetic system, animal welfare calls for less Nikolaidis J, Hoyle I, Kestin S, and of other vertebrates [25] [26]. One likely about aspects of fish welfare. Behav- Psychological stress and welfare in fish.ARBS ethics, 26(1), 1–6. intensive systems focused on promoting fish Knowles T, 2008. Fin erosion in farmed reason for this is the obvious difficulty in ioural measurements have long been Annual Review of Biomedical Sciences 11, quality of life, use of local products and fish. Fish welfare, 121–149. [27] Key B, 2016. Why fish do not feel empathizing with fishes. The aquatic envi- used to assess the organic functioning 1–20. avoidance of live fish transport, use of less pain. Animal Sentience, 1(3), 1. ronment where they move, the perceived of fishes. Psychological conditions, on [17] Noble C, Jones H A C, Damsgård B, chemicals in husbandry and adoption of a [8] Bshary R, Brown C, 2014. Fish cogni- anatomical and functioning differences the other hand, were not studied until Flood M J, Midling K Ø, Roque A, Sæther [28] Rose J D, Arlinghaus R, Cooke S J, more behavioural-based type of manage- tion. Current Biology: 24, R947–50. between humans and fishes, and the lack later. B S, and Cottee S Y, 2012. Injuries and Diggles B K, Sawynok W, Stevens E D, ment. of emotional expressions prevent easy [9] Pottinger T, 2008. The stress response deformities in fish: their potential impacts and Wynne C D, 2014. Can fish really feel In aquaculture, procedures such as human-fish bonds. in fish – mechanisms, effects and meas- upon aquacultural production and welfare. pain? Fish and Fisheries, 15(1), 97–133. Promoting animal welfare in aquaculture is sorting, transport, slaughter and not only an issue for farmers, rather it is urement, in: E.J. Branson (Ed.), Fish Welf., Fish physiology and biochemistry, 38(1), Another important reason for the delay in many others cannot be avoided, but [29] Sneddon L U, 2019. Evolution of noci- a task involving many stakeholders with a Blackwell Publishing, Oxford, UK: pp. pp.61–83. fish acquiring moral status is the divergent they cause disturbance, anxiety and ception and pain: evidence from fish mod- common goal: more sustainable fish produc- 32–48. opinions in relation to their sentience. A sometimes great stress to the fishes. [18] Øverli Ø, Sørensen C, Kiessling A, els. Philosophical Transactions of the Royal tion. Farms should use the best equipment small group of researchers have been fos- Optimal stress management can be [10] Segner H, Sundh H, Buchmann Pottinger T G, and Gjøen H M, 2006. Society B, 374(1785), 20190290. and management practices and adopt good tering a controversy denying the fish ability achieved not only by reducing unnec- K, Douxfils J, Sundell K S, Mathieu C, Selection for improved stress tolerance practice guidelines and certification systems. [30] Balcombe, J 2009. Animal pleasure to feel pain [27] [28]. However, electro- essary stressful procedures (e.g. some Ruane N, Jutfelt F, Toften H, and in rainbow trout (Oncorhynchus mykiss) The academia should promote the identifica- and its moral significance.Applied Animal physiological, behavioural and pharma- handling and transport), but also by Vaughan L, 2012. Health of farmed fish: leads to reduced feed waste. Aquaculture, tion of species-specific needs and validated Behaviour Science, 118 , 208–216. ceutical studies have clearly established modulating the way fishes perceive its relation to fish welfare and its utility as 261(2), 776–781. how fish, like other vertebrates, receive ways to assess welfare on farming fishes. (appraise) some of their stressors. welfare indicator. Fish physiology and bio- [31] Verbeke W, Vanhonacker F, Sioen I, [19] Braithwaite V A, Ebbesson L O E, and process noxious stimuli at brain level, Governmental and non-governmental agen- However, a model farm should not chemistry, 38(1), 85–105. Van Camp J, and De Henauw S, 2007. 2014. Pain and stress responses in farmed and respond with non-reflexive behaviour cies should promote consumer’s education only aim to minimise stress, but should Perceived importance of sustainability and [11] Scott E M, Nolan A M, Reid J, and fish. Rev Sci Tech, 33(1), 245–253. in order to avoid getting hurt [29]. Indeed, and offer appropriate guidelines as well as also promote ways in which the ani- ethics related to fish: A consumer behavior rules and how to implement them. But the Wiseman-Orr M L, 2007. Can we really more than twenty years of research have mals experience a good quality of life. [20] Schreck C B, Jonsson L, Feist G, perspective. AMBIO: A Journal of the last word in this complex system definitely measure animal quality of life? Methodolo- found astonishing advanced and highly and Reno P, 1995. Conditioning improves Human Environment, 36(7), 580–585. belongs to the consumers [31]. They should Promoting animal welfare in aquacul- gies for measuring quality of life in people specialized characteristics in this very di- performance of juvenile Chinook salmon, learn to value local products, and choose ture is not only an issue for fish farm- and other animals. Animal Welfare, 16, verse group of species. They have homolo- Oncorhynchus tshawytscha, to transporta- healthy and balanced diets with a moderate ers, but rather a task involving many 17–24. gous brain structures in comparison to other tion stress, Aquaculture. 135 99–110. vertebrates, they form long-term memories, fish consumption. And they should also learn stakeholders from fish farmers to con- social species learn with each other and how they can, with their choices, promote a sumers, with the common goal of adjust behaviour accordingly, they can use fairer relationship with the fishes they seek more sustainable fish production. tools, etc.. The bulk of present information as a protein source in their dish.

28 I FROM THE RESEARCH I 29 FROM THE RESEARCH

aquaculture takes priority in ensuring better ourally characterised by territorial control, reactive individuals might be better equip- hand, twice per day (09:30 and 15:30). novel object and the remaining area, Coping styles, a tool rearing conditions and quality of life for the active avoidance, and aggression, and ped to cope with a changing or unpredic- The order of feeding was randomized for which were marked with a text marker to better understand animals being farmed. However, funda- physiologically by low hypothalamus-pitui- table environment (e.g. sea cages), as they every meal. Five pellets were added at the on the bottom of the tank (Figure 2c). Fish fish welfare mental insights are lacking on whether and tary-adrenal (HPA axis) reactivity to stress, are more flexible and react more adequately start of feeding and replaced by new ones behaviour was video recorded (SONY, how fish are coping with acute and chronic and low parasympathetic reactivity, while to environmental stimuli. as soon as they were consumed; the num- DCR-SR190E, Japan) for posterior stressors in aquaculture rearing conditions. sympathetic reactivity is high. In contrast, ber of pellets eaten by each fish were noted. analyses. Cameras were placed above Maria Filipa Castanheira, PhD Understanding how animals respond to reactive individuals are behaviourally cha- Feeding continued for a maximum of 1 h, the tanks. The observation period lasted stress in aquaculture is extremely important, Independent Welfare Consultant What are coping styles? racterised by immobility, passive avoidance, after which the remaining pellets were 15 minutes and started immediately after as proactive and reactive fish will differ in (former member of the Fish Ethology and low levels of aggression, and physio- collected and counted. Feeding recovery the novel object was dropped in the tank. Coping styles can be defined as the con- their coping strategies and perception of and Welfare Group), logically by an increase in HPA reactivity, was determined as follows: feeding laten- During the 15 min observation period sistent individual variation in behaviour, external events. Consequently, while one in- Carrer de Benet Cortada 58,1,1 high parasympathetic reactivity, and low cy (time in seconds taken by each fish to the following parameters were mea- physiology, and cognitive/emotional pat- dividual may interpret a situation as being 08174 Cugat del Valles, Spain sympathetic reactivity [5]. Coping styles consume the first pellet); total feeding time sured: latency to enter the 5 cm and 10 cm terns. In animals, including fishes, consistent highly stressful, another may interpret it as [email protected] are shaped by evolution and are adaptive (total time in seconds taken by each fish radius areas (time in seconds taken by individual differences in several aspects of mildly stressful or even as not at all stressful. response patterns to challenges in the natural to consume all pellets until apparent sati- each fish to enter in each area) and the Today, fish welfare is a buzz word for stress responsiveness have been associated environment, so different patterns according ation); number of feeding acts (number of number of times a fish entered in each area. the aquaculture industry, not just for public with differences in behaviour and physiology How to measure coping styles in to different environments are expected. In times an individual approached the pellets The entrance in the area was defined perception, marketing and product accep- [1] [2] [3] [4]. These individual differences farmed fish? a stable environment, proactive individuals resulting in feed consumption), number of when the snout of the fish was inside tance, but also often in terms of production may reflect distinctcoping styles (often also are characterised by easily developing rou- During my PhD works I investigated whe- feeding days (number of feed intake days) the area. efficiency, quality, and quantity. Many aqua- referred to as personalities, temperament, tines and a rigid type of behaviour, which ther individual differences in behavioural and feed intake (in % of body weight). culture practices such as transport, handling, behaviour syndromes, bold/shy continu- Restraining test might be an advantage in an aquaculture responses to a variety of challenges can be feeding techniques, human presence, and um). In fishes, two main coping styles cate- Novel object test stable rearing systems (e.g. recirculation used to assess personality in fish. Several The net restraining test (day 9, after onset stocking densities, potentially elicit acute and gory types are recognised: proactive and aquaculture systems, RAS). In contrast, tests were developed (Figure 1): feed intake The novel object test (day 8, after onset of isolation, last day of individual-based chronic stress responses. Thus, responsible reactive. Proactive individuals are behavi- recovery in a novel environment, novel ob- of isolation) consisted of a Lego® brick tests) consisted of holding each fish individ- ject, restraining, risk-taking and hypoxia (3 cm length x 3 cm width x 2.3 cm height ually in an emerged net for three minutes [6]. These tests focus on one personality – used during the dimension: the exploration-avoidance [7]. first run, Figure 2a) 2c Gilthead seabream (Sparus aurata) was or a table tennis used as a model species, as it is widely ball filled with sand used in research due to its robustness and (2 cm radius —used well-known biology and behaviour. It is during the second also ranked second as the most important run, Figure 2b) that European farmed fish. were dropped sud- denly in the middle Individual-based tests (Figure 1) of the tank. The bot- Feeding recovery test tom of the test tanks was divided into The feeding recovery test consisted of the three distinct zones: daily feed intake by fishes housed in isola- 5 cm and 10 cm tion for 7 days. Fish were fed ad libitum, by radius around the

2a 2b

Figure 1: Schematic representation of the experimental set-up used to determine personality in Gilthead seabream (Sparus aurata). Daily feed intake recovery on isolated fish (n=24) was recorded during 7 days. On days 8 and 9 the same fish were submitted to the novel object test and the net restraining test, respectively. Each test was repeated twice (run 1 and run 2) with an interval between runs of 14 days. Individual- Figures 2a, 2b and 2c: Novel object tests (Photos: MF. Castanheira). based tests were run first (both run 1 and 2) followed by the grouped-based tests.

30 I FROM THE RESEARCH I 31 FROM THE RESEARCH

(Figure 3), while the following behaviours antennas started to register the fish move- Fish behaviour was recorded on video responsiveness) are clearly beneficial un- active individuals showed lower growth than Fish welfare and stress were measured: latency to escape (time in ment between sides. The dissolved oxygen (MicroVideo™ camera MCV2120-WP- der aquaculture conditions. Also, Killen the intermediate [21]. This promotes the idea In most fish species, chronic or acute stress seconds taken by each fish to show an es- in the water (DO) was measured by an LED, Canada) for subsequent measurement et al. [9] reported that in Sea bass, the that selection criteria should perhaps favour is considered as the main factor reducing cape attempt; escape attempt was defined Oxyguard handy probe (Handy Delta, of: latency for risk-taking (time in seconds amount of risk-taking among individuals individuals with intermediate coping styles animal welfare in intensive husbandry pro- as an elevation of the body from the net); USA). During the hypoxia test, fish behav- taken by each fish to enter the risk area); was positively correlated with their rou- characteristics, avoiding the proactive and ductions [15][26]. It is accepted that some number of escape attempts, and total time iour was recorded on video (MicroVideo™ order of risk-taking and number of returns tine metabolic rate. However, Martins et reactive extremes. The same was verified in individuals passively withdraw from poten- spent on escape attempts (total time in sec- camera MCV2120-WP-LED, Canada) for (number of times an individual returns to the al. [10] have reported opposite results in a small ongrowing Sea bass farm in Slove- tially harmful stimuli (i. e., reactive), whereas onds taken by each fish escaping since the posterior analyses. The following behav- safe area after dwelling in the risk area). metabolic rate (oxygen consumption) meas- nia, where the selection of the larvae for the others actively avoid or try to fight harmful first to the last escape attempts). iours were measured: latency to escape The risk-taking test was finalised when half ured when Senegalese sole were housed ongrowing site was based on intermediate and challenging situations (i. e., active). hypoxia (time in seconds taken by each of the fish entered in the risk area or 4.5 in respirometry chambers. These authors growing characteristics [22]. Consequent- However, despite the link between acute Group-based tests (Figure1) fish to escape hypoxia conditions); order of hours after the beginning of the experiment. suggested that different individuals reacted ly, selection programmes in the aquaculture response to challenges and coping styles, Hypoxia test escape and number of returns (number of differently when housed in the metabolic industry have recently included ‘decreased very little information is available about chro- times an individual returned to the hypox- What are the consequences of chambers that functioned as confinement within-population deviation in growth’ as a nic stressors and coping styles. For example, The hypoxia test consisted of reducing the ia side after being in the normoxia side). different stress coping styles in chambers. Individuals that consumed less desirable trait. Korte et al. [27] observed that adaptive pro- oxygen levels in one side of a two-chamber The hypoxia test was finalised when half farmed fishes for aquaculture? oxygen in a respirometry chamber were cesses, i.e., actively maintenance of stability tank and measuring the escape behaviour of the fish escaped from the hypoxia side The presence of coping styles may have also the individuals that reacted sooner to Disease resistance and parasites through change (allostasis), are dependent from the hypoxia to the normoxia side. The or when a concentration of 3 mg/L DO several implications for aquaculture. In- a confinement stress (typical behaviour of Another important implication of coping on the personality type and associated stress tank was composed of two similar circular 3 was reached. dividual fishes within a population often proactive individuals). This apparent con- styles in farmed fishes is the different dis- responses. The benefits of allostasis and the tanks (40 L) that were connected with a differ in how strongly they respond, behav- tradiction may have to do with the passive ease susceptibility exhibited by proactive costs of adaptation (allostatic load) may lead transparent plastic pipe (40 cm length x Risk-taking test iourally and physiologically, under stress benthic lifestyle of sole, compared to other and reactive individuals. Diseases are one to different trade-offs in health and stress 6 cm radius, Figure 1). In the extremes of The risk-taking test was done in a 300 L conditions. A failure to accommodate the more active fish species, highlighting the of the main challenges in aquaculture and related diseases, reinforcing the fact that the connection pipe two circular antennas fibreglass tank (100 cm length x 60 cm coping styles of fishes under farming con- fact that individuals may interpret the same can cause a considerable financial burden both coping styles (proactive/reactive) can were placed (diameter 100/125 x 20 mm width x 50 cm depth) separated in two ditions can lead to problems linked with situation in different ways. to the farmer. Early studies on inflammato- be successful, under different environmen- Trovan®, Netherlands) to allow indivi- distinct areas: safe and risk areas. The production (e.g. aggression, growth, and ry challenges with bacterial pathogens re- tal conditions. Undoubtedly, coping styles dual tracking of the fish passing through areas were divided using a solid plas- disease resistance). Selection programmes ported distinct disease resistance between play an important role in understanding how the pipe (Figure 4). Each side of the tank tic partition (2 mm thickness) with a hole Selection programmes in farmed fish are ex- coping styles [23] [24] [25]. Fevolden et different individuals appraise the housing was equipped with water inflow, outflow (6 cm radius), connected to a circular anten- Growth performance tremely important and focus essentially on al. [23] suggested selection by targeting environment and thereby their welfare status. and air stone supply. The connection ® na, diameter 100/125 x 20 mm (Trovan , and energetics growth performance [11]. As seen before, distinct coping styles rather than for specific pipe was closed with a removable door Netherlands) that allowed the identification Knowing that farmed fishes have coping One of the best examples of the implica- proactive individuals exhibit fast growth but immune traits, selecting for a broad spec- (13 cm length x 13 cm width) before the of which fish passed through the hole and styles and that coping styles differ in how coping have also shown to be more aggressive trum of defence mechanisms and hence start of the test. Each group of fish (n =12) tions of styles in performance traits they appraise their environment may help the time of each passage. The connection [12] [13] [14]. Therefore, we also need affecting resistance to several diseases. was allowed to settle overnight in one side comes from studies with African catfish[8] in the design of farming environments that hole was closed with a removable door to be aware that selection for fast growing Moreover, MacKenzie et al. [25] showed (side 1) before the start of the experiment. that showed that the most efficient individ- are more diverse and could improve the (13 cm length x 13 cm width). Each group individuals may result in co-selection of un- distinct regulation of proinflammatory gene At the beginning of the experiment the wa- uals were those that reacted quicker to the welfare of individuals with different cop- of fish (n =12) was allowed to settle over- desirable traits such as aggression. Actual- expression suggesting that fundamental ter supply was stopped on both sides. Aera- presence of pellets and consumed their ing styles. In turn, this may increase pro- night in the safe area before the start of ly, aggressiveness has been linked with a differences in cytokine regulation exist in tion on side 1 was turned off and replaced meals faster after transfer into a novel envi- duction output and decrease vulnerability the experiment. At the beginning of the ex- diversity of aquaculture problems including fishes with distinct coping styles. by nitrogen which leads to a gradual de- ronment. These individuals were also those to disease. In general, the range of the periment the door was removed and decreased feed intake, growth dispersion, crease in oxygen concentration (Figure 1). that exhibited a lower cortisol response Among the diseases, Salmon lice is consi- coping style spectrum that leads to maxi- 10 pellets (6 % of body weight) were re- chronic stress and disease vulnerability Afterwards, the door blocking the connec- after acute stress. All these characteristics dered the major threat to marine farming of mum growth performance, highest welfare leased into the risk area every 5 minutes [15], reinforcing the possible co-selection tion tube was removed and the circular (better feed efficiency and lower stress salmonids [43]. Øverli et al. [44] showed conditions, and disease resistance may to stimulate fish going to the risk area. of undesirable traits during broodstock se- that salmons with higher black skin spots change depending on the husbandry sys- lection. Furthermore, fighting brings a sig- harboured fewer mature female lice carrying tem, because different types of intensive, nificant cost in terms of increased energy egg sacs, suggesting that individual host semi-intensive or extensive systems present expenditure that may promote inefficient traits may decrease parasite infestation. very different social and environmental con- growth. In addition, aggression among Moreover, the same authors also demons- ditions to fishes. Therefore, individual vari- fishes in production systems can be a cause trated that the presence of sea lice affects ation in the threshold for when a challenge of skin and fin damage. This damage can behaviour and brain serotonergic activity becomes inhibiting rather than stimulatory directly reduce the value of the farmed in Atlantic salmon. Also, Kittilsen et al. [51] is likely correlated with how a specific indi- product and increase the vulnerability to provided evidence for individual variation vidual is coping with a welfare issue within diseases. Moreover, proactive individuals in parasites resistance to sea lice, particu- a particular situation. have also been shown to develop routines larly salmon louse (Lapeophtheiras salmonis) more easily [16] [17] [18] [19] [20]. Such carrying egg sacs. Are coping styles for life? characteristics may be more advantageous under stable conditions provided by inten- The few studies above have not investiga- Social context sive husbandry systems but prejudicial in ted the correlation between immune reac- A pertinent topic is also to understand if extensive or semi-intensive husbandry sys- tivity, individual variation, and associated coping styles are maintained lifelong. For tems with lower standardised conditions. mechanisms. This underlines the need for example, are coping styles influenced by fundamental studies to understand individual Figure 3: Fish in the restraining test (Photo: MF. Castanheira). Figure 4: Fish in the hypoxia test. Individual tracking of the tagged In farmed rainbow trout, where coping styles the social context of a fish's development disease vulnerability. fish was possible with the help of a PIT antenna were characterised by the time period until stage? This was also something that I took (Photo: MF. Castanheira). first feeding, both the proactive and the re- a look into during my PhD work [28],

32 I FROM THE RESEARCH I 33 FROM THE RESEARCH

trying firstly to understand if the consisten- [5] [12] [13] [39] [40] [41] [42]. On the References effects on risk-taking in individual juvenile [19] Frost AJ, Winrow-Giffen A, Ashley P J, Take Home Message cy of escape behaviour, one of the main other hand, personality types can be modi- [1] Øverli Ø, Sørensen C, Pulman K G T, European sea bass. Journal of Animal and Sneddon L U, 2007. Plasticity in animal dimensions of personality in animals, fied by the influence of other group mem- Pottinger T G, Korzan W, Summers C H, Ecology 80(5): 1024–33. personality traits: does prior experience al- remained consistent under different so- bers [45] [46] [47]. The presence of coping styles is now ter the degree of boldness? Proceedings of and Nilsson G E, 2007. Evolutionary back- [10] Martins C I M, Castanheira M F, cial contexts, i.e. if other group members well recognised in farmed fishes and its the Royal Society B: Biological Sciences ground for stress-coping styles: Relationships Engrola S, Costas B, and Conceição L E C, influence the consistency of individual Life stage influence implication for aquaculture can be as 274: 333–339. between physiological, behavioral, and 2011d. Individual differences in metabolism avoidance behaviour. Here, the escape/ wide as reviewed here. Taken together, Another question that might pop up when cognitive traits in non-mammalian verte- predict coping styles in fish. Applied Animal [20] Höglund E, Silva P I, Vindas M A, and avoidance response during the restrain- the extensive literature on coping styles studying the coping styles in fishes is if they brates. Neuroscience and Biobehavioral Behaviour Science 130: 135-143. Øverli Ø, 2017. Contrasting coping styles ing test indicated a consistent personality in fish shows that screening for coping are consistent during the whole lifecycle, Reviews 31: 396–412. meet the wall: a dopamine driven dichotomy trait in intermediate and control groups: especially in those species that suffer deep styles is species-specific. The recent de- [11] Gjedrem T, 2005. Selection and [2] Réale D, Dingemanse N J, Kazem in behavior and cognition. Front Neurosci individuals showing lower latency to es- biological changes (e.g., sexual reversion). velopment of group-based tests and the Breeding Programs in Aquaculture, 364 p, A J N, and Wright J, 2010a. Evolutionary 11:383. cape, higher number of escape attempts Therefore, one of the objectives of my PhD use of proxies may provide an oppor- Springr. and spending more time escaping during tunity for mass screening in the future. and ecological approaches to the study of [21] Andersson M Å, Laursen D C, Silva was also to characterise fish coping styles [12] Øverli Ø, Korzan W J, Höglund E, the initial screening, showed a similar Mass screening into different coping personality. Philosophical Transactions of the P, and Höglund E, 2013. The relationship considering the consistency of behavioural Winberg S, Bollig H, Watt M, Forster G L, behaviour after one month when the test styles may help optimise the production Royal Society B: Biological Sciences 365: be-tween emergence from spawning gravel responses over time and during life history Barton B A, Øverli E, Renner K J, was repeated. In proactive and reactive systems as optimal conditions for pro- 3937–3946. and growth in farmed rainbow trout Onco- using the behavioural responses during a and Summersa C H, 2004a. Stress coping groups, no correlation was found. Several active individuals are likely to be differ- rhynchus mykiss. Journal of Fish Biology net restraining test and cortisol responsive- [3] Réale D, Garant D, Humphries M M, style predicts aggression and social dom- studies suggest that social context strongly ent from those for reactive individuals. 83:214–219. ness at distinct life history stages [48]. We Bergeron P, Careau V, and Montiglio P O, inance in rainbow trout. Hormones and influences the individual personality [29]. found consistency in behavioural responses In addition, the recognition that farmed 2010b. Personality and the emergence of Behavior 45: 235–241. [22] Fonda I, 2018. Personal communica- Social context is involved in the regulation (over time) during the restraining test until fishes exhibit coping styles means that the pace-of-life syndrome concept at the tion. [13] Øverli Ø, Korzan W J, Larson E T, of numerous characteristic behaviours such 8 months after the first screening. Howev- several behavioural and physiological population level. Philosophical Transactions Winberg S, Lepage O, Pottinger T G, [23] Fevolden S E, Refstie T, and Røed K H, as social facilitation [30], social familiarity er, during sexual maturation this escape responses will vary as part of a com- of the Royal Society B-Biological Sciences Renner K J, and Summersa C H, 2004b. Be- 1992. Disease resistance in rainbow trout [52], social dominance [31], social plas- behaviour consistency under restraining mon ‘package’ that should be taken 365: 4051–4063. havioral and neuroendocrine correlates of (Oncorhynchus mykiss) selected for stress ticity [32] [33], and social learning [34]. was lost. This lack of consistency found in into consideration when designing se- [4] Silva P I M, Martins C I M, Engrola S, displaced aggression in trout. Hormones response. Aquaculture 104: 19–29. For example, the presence of conspecif- coping styles across life stages is a new lection programmes. Marino G, Øverli Ø, and Conceição L E C, and Behavior 45: 324–329. ics may cause individuals to enhance or important finding and suggests that differ- [24] Fevolden S E, Nordmo R, Refstie T, suppress threat-sensitive behaviour such as Measuring fish welfare in the context 2010. Individual differences in cortisol levels ences in coping styles expressed at early [14] Castanheira M F, Herrera M, Costas and Røed K H, 1993. Disease resistance in activity, exploration/risk, foraging, feeding of individual variation in coping ability and behaviour of Senegalese sole (Solea developmental stages may change accord- B, Conceição L E C, and Martins C I M, Atlantic salmon (Salmo salar) selected for rate, and courting opportunities [35] [36] was assisted by some studies of differ- senegalensis) juveniles: Evidence for coping ing to age and life history experiences. 2013a. Linking cortisol responsiveness high or low responses to stress. Aquaculture [37] [38]. Furthermore, individuals with ex- ences in central nervous system func- styles. Applied Animal Behaviour Science This highlights the fact that coping styles and aggressive behaviour in Gilthead sea- 109: 215–224. tions between proactive and reactive 124: 75–81. treme personality types may be affected in are not fixed and this can be reflected in bream Sparus aurata: Indication of divergent individuals [49] [50]. In aquaculture [25] MacKenzie S, Ribas L, Pilarczyk M, a different way. Our results therefore sug- distinct behavioural strategies to cope with [5] Koolhaas J M, Korte S M, De Boer S F, coping styles. Applied Animal Behaviour rearing conditions, these differences Capdevila DM, Kadri S, and Huntingford gested the potential influence of the social the same stressful condition. Thus, different Van Der Vegt B J, Van Reenen C G, Science 143: 75-81. in the nervous system must be included context in fishes. This is a finding that can life stages could mean a paradigm shift in Hopster H, De Jong I C, Ruis M A W, FA, 2009. Screening for Coping Style somehow when gene and environmen- be explained by the fact that individuals the coping styles field and the following hy- and Blokhuis H J, 1999. Coping styles [15] Ashley P J, 2007. Fish welfare: Current Increases the Power of Gene Expression tal interactions are explored to evaluate tend to adjust their social behaviour ac- potheses may be considered to contribute in animals: current status in behavior issues in aquaculture. Applied Animal Behav- Studies. PLoS ONE 4: e5314. the stability of welfare relevant trait cor- iour Science 104: 199–235. cording to the available social information to this lack of consistency in escape behav- and stress-physiology. Neuroscience and [26] Huntingford F A, Adams C, Braith- relations. in the group, to adjust and optimise their iour responses: Biobehavioral Reviews 23: 925–935. [16] Ruiz-Gomez M L, Kittilsen S, Höglund waite V A, Kadri S, Pottinger T G, own personality type. These adjustments However, coping styles screening is far 1) the sexual maturation and the sex inver- [6] Castanheira M F, Herrera M, E, Huntingford F A, Sørensen C, Pottinger Sandøe P, and Turnbull J F, 2006. Current could have an ecological and evolution- from being used in daily aquaculture sion process compromise the consisten- Costas B, Conceição L E C, and Martins TG, Bakken M, Winberg S, Korzan W J, issues in fish welfare. Journal of Fish Biology ary significance related to adaptation to practice due to lack of knowledge and/ cy of coping styles abilities or/and C I M, 2013b. Can we predict personali- and Øverli Ø, 2008. Behavioral plastici- 68: 332–372. new environmental conditions. The under- or the time required. More awareness ty in rainbow trout (Oncorhynchus mykiss) ty in fish? — searching for consistency over [27] Korte S M, Koolhaas J M, Wingfield standing of these differences may have 2) the contextual importance of the net re- and a practical approach to on the with divergent coping styles: When doves time and across contexts. PLoS ONE 8(4): J C, and McEwen B S, 2005. The Darwinian several practical implications. One exam- straining response may differ according topic should be addressed in the near become hawks. Hormones and Behavior e62037 concept of stress: Benefits of allostasis and ple is the possibility to take advantage of to age and fish development. future. 54: 534-538. this social behaviour and develop rearing [7] Champagne D L, Hoefnagels C C M, costs of allostatic load and the trade-offs in conditions accordingly. For example, the de Kloet R E, and Richardson M K, 2010. [17] Ruiz-Gomez M L, Huntingford F A, health and disease. Neuroscience and Bio- aquaculture industry may take advantage Translating rodent behavioral repertoire to Øverli Ø, Thörnqvist P-O, and Höglund E, behavioral Reviews 29: 3–38. 2011. Response to environmental change of this group heterogeneity in semi-inten- zebrafish(Danio rerio): Relevance for stress [28] Castanheira M F, Cerqueira M, Millot in rainbow trout selected for divergent stress sive and extensive conditions where the research. Behavioural Brain Research 214: S, Gonçalves R A, Oliveira C, Conceição coping styles. Physiology & Behavior 102: individuals are more susceptible to environ- 332–342. L E C, and Martins C I M 2016a. Are per- mental changes (i.e. in a changing envi- 317–322. [8] Martins C I M, 2005. Individual vari- sonality traits consistent in fish? — The in- ronment, the social support may result in ation in growth of African catfish Clarias [18] Basic D, Winberg S, Schjolden J, fluence of social context.Applied Animal a potential boost of the production, and gariepinus: a search for explanatory factors Krogdahl Å, and Höglund E, 2012. Context- Behaviour Science 178: 96101.­ the performance of some individuals may dependent responses to novelty in Rain- (Phd thesis). Wageningen University, The [29] Webster MM, Ward AJ, 2011. Person- be reflected in a faster growth. On one bow trout (Oncorhynchus mykiss), selected Netherlands. ality and social context. Biological Reviews hand, our results comply with previous stud- for high and low post-stress cortisol respon- 86: 759–77. ies indicating the presence of personality [9] Killen S S, Marras S, and McKenzie D J, siveness. Physiology and Behaviour 105: types that seemed based on innate traits 2011. Fuel, fasting, fear: routine metabolic 1175–1181. rate and feed deprivation exert synergistic

34 I FROM THE RESEARCH I 35 FROM THE RESEARCH FROM THE RESEARCH

[30] Webster M M, Ward A J W, and [42] Millot S, Bégout ML, and Chatain B, [52] Galhardo L, Vitorino A, Oliveira RF, food safety, equilibrated diets, exercise, or is an increase of disease incidence and Hart P J B, 2007. Boldness is influenced 2009b. Risk-taking behaviour variation over 2012. Social familiarity modulates person- Fish welfare: avoiding stress are included among other consequently, loss of welfare [3] [4] [5]. by social context in threespine sticklebacks time in sea bass Dicentrarchus labrax: ef- ality trait in a cichlid fish.Biology Letters 8: Interconnections among healthy habits. In this way, stress indicators may reason- (Gasterosteus aculeatus). Behaviour 144: fects od day-night alterations, fish phenotipic 936–938. ably help to characterise a welfare status, stress, health, environ- These concepts can also be applied to 351–371. characteristics and selection for growth. provided that the stress physiology of fishes ment and diversity farm animals including fishes, thus ap- Journal of Fish Biology 75: 1733–1749. has been studied for decades [6] and indi- [31] Montero D, Lalumera G, Izquierdo proaching even more closely the health cators of different nature (concerning phys- M S, Caballero M J, Saroglia M, and Tort L, [43] Johnson S C, Treasurer J W, Bravo S, and the welfare features. As an example, Lluis Tort (Prof.), iology, metabolism, genome, behaviour, 2009. Establishment of dominance relation- Nagasawa K, Kabata Z, 2004. A review some episodes of sudden death in Sea Joan Carles Balasch (Dr.) performance, etc.) are available. ships in gilthead sea bream Sparus aurata of the impact of parasitic copepods on ma- bass during the nineties in South Mediter- juveniles during feeding: effects on feeding rine aquaculture. Zoological Studies 43 (2): Universität Barcelona, ranean sea cages could have been clearly Perceiving stress behaviour, feed utilization and fish health. 229–243. Autonomous University of Barcelona, associated with non-pathogenic sources Journal of Fish Biology 74: 790–805. Department of Cellular Biology, like fatty diets and reduced exercise as a How fishes perceive stressors is very rel- [44] Øverli Ø, Nordgreen J, Mejdell C M, Physiology and Immunology, result of pressure for fast growth and higher evant in terms of developing a response, [32] Oliveira R F, 2009. Social behavior in Janczak A M, Kittilsen S, Johansen I B, Campus Bellaterra, culture densities [1]. This situation involved for reacting in a particular way and for the context: Hormonal modulation of behavioral Horsberg T E, 2014. Ectoparasitic sea lice 08193 Cerdanyola del Valles, Spain reduced welfare as a result of the lack of recovery of a welfare status, physiological plasticity and social competence. Integrative (Lepeophtheirus salmonis) affect behaviour [email protected] healthy habits infringed on fish. balance and maintaining overall health. and Comparative Biology 49: 423–440. and brain serotonergic activity in Atlantic [email protected] Fishes are animals intensively connected salmon (Salmo salar L.): Perspectives on an- Welfare in animals including fishes has with the environment with many recep- [33] Oliveira R F, 2012. Social plasticity in In this paper the connections between imal welfare. Physiology & Behavior 132: been most often associated with the lack tors associated with the changes in biotic fish: Integrating mechanisms and function. welfare, stress and health in fishes are dis- 1 44–50. of suffering and with the Five Freedoms and abiotic features of the water and the Journal of Fish Biology 81: 2127–2150. cussed briefly in relation to the relevant fac- [2], and particularly to episodes of eutha- characteristics of the organisms living in it. [45] Magnhagen C and Staffan F, 2005. tors affecting this connection, such as the [34] Brown C and K N Laland, 2003. nasia and anaesthesia in aquaculture har- Therefore, temperature, ionic and osmotic Is boldness affected by group compo- variability and diversity among fish species Social learning in fishes: a review. Fish and vesting or fish transport with trading fish in components, currents, but also all types of sition in young-of-the-year perch (Perca and the ability to adapt to different environ- Fisheries 4: 280–288. aquariology. Nonetheless, when it comes pathogenic and non-pathogenic microor- fluviatilis)? Behavioral Ecology and Socio- ments, the individuality in coping strategies to measuring welfare and determining suit- ganisms are in constant interaction with the [35] Schuett W, Godin JGJ, and Dall SRX, biology 57: 295–303. and behaviour, and the variety and capac- able indicators, the welfare criteria used fish, and in particular to external fish sensors 2011. Do female zebra finches, Taeniopygia ity of sensoring the environment. This paper [46] Magnhagen C, 2007. Social influence to match with the lack of stress, as stress and mucosal surfaces. In recent years it has guttata, choose their mates based on their focuses on the proximity of the content on on the correlation between behaviours in includes most of the situations in which fish- been shown that mucosae (skin, gut, gills ‘personality’? Ethology 117: 908–917. the concepts of health and welfare, espe- young-of-the-year perch. Behavioral Ecology es experience a significantly altered status and nasal) are key sites for fish-environment cially when applied to indicators on how to [36] Schuett W, Tregenza T, andDall S R X, and Sociobiology 61: 525–531. (Figure 1), from mild alarm to eventual suf- interaction and therefore relevant agents 2010. Sexual selection and animal personal- measure and manage welfare and health. fering. When fishes are stressed, as hap- [47] Magnhagen C and Bunnefeld N, in the modulation of the transitions be- ity. Biological Reviews 85: 217–246. pens with most vertebrates, there is an in- 2009. Express your personality or go along tween welfare and health status and stressed Stress, welfare, and health crease of susceptibility to pathogens, there [37] Cote J, Fogarty S, Weinersmith K, with the group: what determines the behav- and pathological [7]. The assessment of Welfare is a concept with many connec- Brodin T, and Sih A, 2010. Personality traits iour of shoaling perch? Proceedings of the tions with the health concept. Although we and dispersal tendency in the invasive mos- Royal Society B: Biological Sciences 276: normally associate health in animals with quitofish (Gambusia affinis). Proceedings 3369–3375. the lack of disease or the lack of patho- of the Royal Society B: Biological Sciences [48] Castanheira M F, Martínez Páramo gen input, it is normally true that healthy 277: 1571–1579. S, Figueiredo F, Cerqueira, M, Millot S, animals correspond well with animals in [38] Cote J, Fogarty S, Brodin T, Weinersmith Oliveira C, Martins C I M, and Conceição good welfare, i. e. without significant func- K, and Sih A, 2011. Personality-dependent L E C, 2016b. Are coping styles consistent in tional alterations and developing a rather dispersal in the invasive mosquitofish: group the teleost fish Sparus aurata through sexual normal life. It is true that some aspects of composition matters. Proceedings of the maturation and sex reversal? Fish Biology welfare associated with the development of Royal Society B: Biological Sciences 278: and Biochemistry 42(5):1441-52. natural behaviour may not appear in this 1670–1678. health/welfare concept, but it is also true [49] Vindas M A, et al. 2016. Brain sero- that episodes of discomfort, heavy stress or [39] Brelin et al. 2005 tonergic activation in growth-stunted farmed disease can appear in natural conditions. salmon: adaption versus pathology. Royal [40] Huntingford F A, 1976. The relationship Therefore, in most cases such a correlation Society Open Science 3:160030. between anti-predator behaviour and ag- with health/welfare can work. Moreover, gression among conspecifics in the three- [50] Øverli Ø and Sørensen C, 2016. On in humans other concepts exist such as spined stickleback, Gasterosteus Aculeatus. the role of neurogenesis and neural plasticity public health or the ‘one-health’ concept. Animal Behaviour 24: 245–260. in the evolution of animal personalities and Under these concepts, not only is the lack stress coping styles. Brain, Behavior and [41] Millot S, Bégout ML, and Chatain B, of pathologies and the inexistence of dis- Figure 1: Interconnections between stressors and endogenous responses in fish welfare. Evolution 87:167–174. 2009a. Exploration behaviour and flight re- ease considered, but also aspects such as sponse toward a stimulus in three sea bass [51] Kittilsen S, Johansen IB, Braastad BO, strains (Dicentrarchus labrax L.). Applied Øverli Ø, 2012. Pigments, parasites and 1 The concept of the ‘Five Freedoms’ comes from the report of the British Committee of Inquiry into the Welfare of Animals in Intensive Animal Behaviour Science 119: 108–114. personalitiy: Towards a unifying role for ster- Systems (Brambell Report, 1965). Farm animals should have the freedom to ‘stand up, lie down, turn around, groom themselves and oid hormones? PLoS ONE 7 (4): e34281. stretch their limbs’. (Ed.) https://www.canr.msu.edu/news/an_animal_welfare_history_lesson_on_the_five_freedoms

36 I FROM THE RESEARCH I 37 FROM THE RESEARCH

environmental selective pressures that elicit but have the opportunity to increase wel- of gilthead seabream (Sparus aurata), [12] Balasch J C and Tort L, 2019. Netting multilevel responses and produce a meas- fare through abundant feeding or effective Fishes are animals that are intensively zebrafish (Danio rerio) and rainbow trout the Stress Responses in Fish. Front Endo- urable allostatic load in every organism. reproductive success [16]. Fishes also in- connected to the environment and (Oncorhynchus mykiss). Fish & Shellfish crinol (Lausanne) 10, 62. When this coping is successful, fishes are dulge in a panoply of reproductive modes, have many receptors for their per- Immunology 86. [13] Vila Pouca C and Brown C, 2017. able to retain welfare. ranging from gonochorism (separate sexes) ception. Therefore, temperature, ionic [4] Mateus A, Power D, and Canario A, Contemporary topics in fish cognition and to sequential or simultaneous hermaphrodit- and osmotic components, currents, but 2017. Stress and Disease in Fish. In Fish behaviour. Current Opinion in Behavioral Responding to stress ism, with few species being true partheno- also all kinds of pathogenic and non- pathogenic micro-organisms are in Diseases: Prevention and Control Strate- Sciences 16, 46–52. One of the main descriptors of a stress genetic [17]. This diversity also influences constant interaction with the fish. gies, pp. 187–220. situation is the energetic component (as it the onset of physiological responses to [14] Castanheira M F, Herrera M, Costas Mucous membranes are key sites for is for other basic functions or organismic environmental stressors [18]. Individual be- [5] Yada T and Tort L, 2016. Stress and B, Conceição L E C, and Martins C I M, fish-environment interaction and thus performance such as growth, disease resis- havioural preferences, intraspecific sex dif- disease resistance: immune system and im- 2013. Can We Predict Personality in Fish? relevant actors in the modulation of tance or reproduction). Thus, any situation ferences, and combined stressors, such as munoendocrine interactions. In Fish Physio- Searching for Consistency over Time and transitions from the state of well-being of stress, discomfort or lack of welfare can mixtures of toxic chemicals, and changes logy, (Elsevier), pp. 365–403. across Contexts. PLoS One 8. of environmental variables (temperature, and health to the state of stress and be translated in terms of the energetic com- [6] Schreck C B and Tort L, 2016. 1 - The [15] Koolhaas J M, de Boer S F, Coppens salinity) during pathological states, may pathology [7]. ponent. Since all animals and plants follow Concept of Stress in Fish. In Fish Physiolo- C M, and Buwalda B, 2010. Neuroendo- transform adaptive responses to stress into the homeostatic rule, (i. e., to react to any Some fishes can live under extreme gy, C.B. Schreck, L. Tort, A.P. Farrell, and crinology of coping styles: Towards under- maladaptive ones [19]. challenge in order to recover the balance conditions. Thanks to this adaptability, C.J. Brauner, eds. (Academic Press), pp. standing the biology of individual varia- of internal variables and adapt to the envi- almost half of the vertebrate species 1–34. tion. Frontiers in Neuroendocrinology 31, Fish health and welfare ronmental inputs), such a reaction always are fishes, whose ability to overcome 307–321. involves minute or longer term reorganisa- management stressors seems to have been quite [7] Parra D, Reyes-Lopez F E, and Tort L, tion of resources and therefore changes in Since many fishes are subjected to anthro- successful. In defining stress respons- 2015. Mucosal Immunity and B Cells in [16] Vindas M A, Gorissen M, Höglund E, the allocation of available energy (see pogenic sources of potential stress (fish- es in fishes, we should analyse the Teleosts: Effect of Vaccination and Stress. Flik G, Tronci V, Damsgård B, Thörnqvist Figure 2). Therefore, significant alterations eries, aquaculture, fish trading, aquariolo- stress phototope, an adaptive niche Front Immunol 6, 354. P-O, Nilsen T O, Winberg S, and Øverli Ø, et al, 2017. How do individuals cope of the energetic balance as a result from gy, and research), the issue of fish health scenario exposed to selective environ- [8] Kulczykowska E, 2019. Stress Respon- with stress? Behavioural, physiological and Figure 2: The energetic drive in fishes under stressors such as heavy space restrictions, management and welfare management is mental pressure that induces respons- se System in the Fish Skin—Welfare Mea- stress or infection. neuronal differences between proactive flying from predators, aggression, injuries, increasingly becoming a priority for those es at multiple levels and produces a sures Revisited. Front. Physiol. 10. pathogens, or those resulting from discom- involved in these activities. In this way, in- measurable allostatic load in any and reactive coping styles in fish. Journal of fort or mild stressors, can indicate chan- dicators of both welfare and health man- organism. If this coping is success- [9] Helfman G, Collette B, Facey D, and Experimental Biology 220, 1524–1532. Bowen B, 2009. The Diversity of Fishes: selected indicators obtained from specific ges in welfare. In this way, performance agement have been developed [20] and ful, the fishes are able to maintain [17] Wootton R and Smith C, 2014. Re- Biology, Evolution, and Ecology. sensors of these mucosal surfaces can be functions like growth, disease resistance or are still being developed for fishes for the their well-being. productive Biology of Teleost Fishes. Repro- also indicators of welfare and even predic- reproductive capacity will receive less re- objectives of maintenance of good health As many fishes are exposed to poten- [10] Harel I and Brunet A, 2015. The ductive Biology of Teleost Fishes 1–472. tors of welfare alteration [8]. sources, with the consequent impairment or and disease prevention and to obtain a tial stress from anthropogenic sourc- African Turquoise Killifish: A Model for Ex- alteration of the degree of such a performance. welfare standard or even a welfare certifi- [18] Schreck C B, 2010. Stress and fish However, a main drawback for describ- es, the issue of managing fish health ploring Vertebrate Aging and Diseases in cation. When it comes to assessing opera- reproduction: the roles of allostasis and ing a unified and integrated physiological Another aspect of fish diversity that is rele- and welfare is increasingly becoming the Fast Lane. Cold Spring Harb. Symp. tional welfare or health, the indicators used hormesis. Gen. Comp. Endocrinol. 165, stress response in fishes concerns their ex- vant to the response to stressors and chal- a priority for fish stakeholders. Indica- Quant. Biol. 80, 275–279. become increasingly similar. 549–556. treme diversity of lifestyles and ecotypes lenges and therefore to the maintenance of tors for the management of fish wel- [11] Nielsen J, Hedeholm R B, Heinemei- [19] Vargas R, Balasch J C, Brandts I, [9]. Fishes can live under extreme condi- welfare is the individual variability. This fea- fare and fish health have been and er J, Bushnell P G, Christiansen J S, Olsen Reyes-López F, Tort L, and Teles M, 2018. tions including freezing waters, dry ponds ture, that is common to most vertebrates, is are being developed and are becom- J, Ramsey C B, Brill R W, Simon M, and Take Home Message Variations in the immune and metabolic or huge pressures in deep waters; fishes also observed in fishes[13] . Some authors ing increasingly similar in their oper- Steffensen K F, et al, 2016. Eye lens radio- response of proactive and reactive Sparus are able to adapt to changing conditions call it personality, although a better word ational application. (Ed.) carbon reveals centuries of longevity in the As a rule, healthy animals probably aurata under stimulation with Vibrio anguil- such as freshwater-seawater transitions, could be individuality, as personality refers Greenland shark (Somniosus microcephalus). also enjoy good welfare. In most cas- larum vaccine. Sci Rep 8, 17352. low oxygen waters or temperature chang- too directly to human features [14]. Wheth- Science 353, 702–704. es, there is therefore a correlation es; fishes have adapted also to all types er a fish behaves proactively/aggressively [20] Carbajal A, between health and welfare. In a References of feed resources; fishes can show sophis- or reactively when faced with a challenge Reyes-López F E, ‘One Health’ concept, healthy habits [1] Parpoura A C R and Alexis M N, ticated predatory activity or efficient mimet- depends on the individual coping strategy, Tallo-Parra O, Lo- include aspects such as food safe- 2001. Effects of different dietary oils in sea ic strategies. Some fishes, such as African life-story experiences, evolutionary con- pez-Bejar M, and ty, balanced diet, exercise or stress bass (Dicentrarchus labrax) nutrition. Aqua- killifish, live only a few months during the strictions, behavioural plasticity, and social Tort L, 2019. avoidance. When it comes to measur- Com- wet season in dry climates [10], whereas context, provided that there is competition culture International 9, 463–476. ing animal welfare and determining parative assessment other species may live centuries in Green- for space, resources or reproductive part- [2] Huntingford F A and Kadri S, 2008. appropriate indicators for this, the of cortisol in plas- land cold waters [11]. This adaptive ability nership [15]. Such diverted behaviour is Welfare and Fish. In Fish Welfare, (John criteria are tailored to the absence ma, skin mucus and has resulted in the fact that almost half of greatly associated with the ability of fishes Wiley & Sons, Ltd), pp. 19–31. of stress, since stress covers most sit- scales as a mea- the existing vertebrate species are fishes. to maintain or recover welfare. Reactive sure of the hypo- uations in which fishes experience [3] Khansari A R, Balasch J, Vallejos-Vidal This fact also shows that the ability of fish- fishes, which have a higher plasticity to thalamic-pituitary-in- a significantly altered status. When E, Teles M, Fierro-Castro C, Tort L, and es to overcome stressors has been quite confronting novel environments, may be- terrenal axis activity fishes are stressed, their susceptibility Reyes-López F, 2018. Comparative study of successful. As recently pointed out [12], come inactive or shy, thus avoiding injuries in fish. Aquaculture. to pathogens increases, leading to an stress and immune-related transcript outco- when defining stress responses in fishes we and heavy stress when facing a possible 506:410 – 416 increase in disease incidence and con- mes triggered by Vibrio anguillarum bacte- should analyse the stressotope, an adap- episode of aggression. On the other hand, sequently to a loss of welfare. rin and air exposure stress in liver and spleen Hatchery in a northern Italian trout farm (Photo: © Studer / fair-fish) tive niche-related scenario subjected to proactive fishes may take much more risk

38 I FROM THE RESEARCH I 39 FROM THE RESEARCH

or to the particular characteristics of the Physical or structural enrichment behaviour of fishes in captivity (e. g. Structural enrichment at application of these structures at commer- at farms aggressiveness, susceptibility to diseas- fish farms: the science cial scale, given that EE strategies must be Structural EE can be defined as a strategy es, swimming activity, cognitive capacity, and the fiction designed according to the species’ needs, to add physical complexity with structures, exploration, appetite, growth rate, physi- life-stage, farming/husbandry system and objects or any structural modification to cal condition, deformities, survival rates). fish densities, and farming conditions and These effects often vary in direction and Pablo Arechavala-Lopez (Dr.) increase heterogeneity of the rearing en- needs. From the fish-farmers’ point of view, vironment [10]. This kind of EE is based magnitude, and each species and stage Fish Ethology and Welfare Group, if structural EE can increase fish growth and on the fact that some fish species use the of life needs special consideration with re- Centro de Ciencias do Mar (CCMAR), improve final product quality, as well as floor substrate or shelters in their natural en- spect to its natural history and preferences. Rua José Mateus Horta 3, welfare conditions, they might get econom- vironment, and therefore, they might also However, it is of special concern for fish 38000-536 Faro, Portugal ic and ethical benefits. Fish welfare is an frequently make use of structural enrichment farmers that the application of structural EE [email protected] important issue for the industry, not only be- when held in captivity. Enrichment struc- in the farming system can be also associat- cause of public perception, commercializa- tures can be built with a wide variety of ed with some problems, compromising the Environmental enrichment: tion and acceptance of products, but also products, shapes and sizes. However, it is health and well-being of fishes. The natural concepts and relevance because of benefit in terms of efficiency, Figure 1. Schematic representations of simple structural enrichment with hanging ropes made of special concern for fish farmers that the environment cannot be exactly recreated in quality, and quantity of production [7]. of plant fibres, which can be used in rearing tanks (A) and ongrowing sea-cages Environmental enrichment (EE) can be application of structural EE in the farming the hatcheries, so the objective when de- (B) to improve the welfare conditions of Sea bream (modified from [49] and [50]). generally defined as‘the stimulation of the system can be also associated with some signing enrichment is to modify elements of Environmental enrichment brain by its physical and social surround- problems (e.g. food particles and faeces the artificial environments in order to pro- and farmed fishes ings’. Looking for a more applied definition accumulation, inadequate designs and vide welfare benefits without compromising into the animal world, some authors under- The farming facilities are generally desig- materials, neophobia, territoriality, etc.), substrates helped to reduce fin and skin are already available on the market and the biosecurity of the farms. For example, stand EE as altering the living environment ned and constructed to optimize growth and compromising the health and well-being of erosion and decrease infections [14] [16] implemented in most of the salmon hatch- some structures or objects can accumulate of captive animals in order to provide op- health, and therefore, on the basis of eco- fish. It is necessary, therefore, to experimen- [25]. In flatfish species (Hippoglossus hip- eries worldwide. Similar positive effects on food particles and faeces, making clean- portunities to express more of their natural nomic and human ergonomic requirements, tally test the possible effects of the designed poglossus, Solea solea, Paralichthys oliva- hatchlings have been shown for Atlantic ing and disinfection tasks difficult, and thus behavioural repertoire [1] or improving the with little consideration for animal welfare. structures on the target species, taking into ceus), it also increased resting behaviour, sturgeon (Acipenser oxyrinchus) and White compromise the health and welfare of fish- biological functioning of captive animals The production of fin-fish aquaculture, and account all aspects mentioned above, be- reduced metabolic rate, and decreased sturgeon (A. transmontanus) adding sand es. In these cases, increasing the periodic- from modifications in their environment in particular intensive farming systems, can fore implementing it on a commercial scale. cannibalism [26] [27] [28] [29] [30] and and/or gravel to the bottom of the tanks ity of tank cleaning should be considered [2] based on understanding the animal’s cause welfare problems such as stress, Among structural EE, 4 different types can also reduced or eliminated ambicoloura- [36] [37] [38] [57]. (e.g. increasing the effort of manual labour natural history [3]. Other authors defined health problems, psychological stress, and be found: shelters, floor substrate, incuba- tion [31] [32]. In the case of Mozambique Structural enrichment can simply add envi- or application of internal filters). EE as a systematic scientific approach even mortality at any stage of the production tion substrate, and habitat complexity. tilapia (Oreochromis mossambicus), sandy ronmental complexity and heterogeneity. to understanding and providing for the process [8] [9]. Rearing environments in fish bottoms can reduce aggressiveness during It can also happen that the structures used Regarding those EE providing shelter to Recent studies on diverse species of salmo- psychological and behavioural needs of farms generally lacks structure, mainly for courtship and nest-building, and therefore, filter out potentially hazardous chemicals captive fishes, there is a wide range of nids have demonstrated that farmers might captive animals [4]. Therefore, taking all practical reasons for the farmer, and stressors reducing stress and increasing welfare of to the environment (e.g. PVC phthalates), studies on different species. For instance, increase fish growth and condition, mod- these aspects into consideration, EE can be in aquaculture, such as handling, transpor- breeding [56]. Similarly, some studies on or that their design is inadequate and caus- some works on catfish species demonstrated ify the water flow and swimming activity defined as‘providing the environmental tation, stocking densities and feeding are Gilthead seabream (Sparus aurata) report- es physical or psychological disturbanc- that simple structures, such as plastic strips by adding aluminium bars and strings of stimuli necessary for optimal behaviour- unavoidable. Reducing both stress and its ed similar positive effects by adding gravel es or damage to the fish (e. g. small holes, or tubes, can provide hiding places, but spheres from the top of the tank [39] [40] al, physiological, morphological and harmful effects is a fundamental goal for to the bottom of the rearing environment, cracks, protrusions, noise), increasing the also increase growth and survival of fish, as [41] [42] [43] [44] [45] [46]. In addi- psycological welfare’. Its objective is to successful growth, production, and welfare but authors shed light on the fact that dif- risk of infections, stress or the mortality rate. well as inhibit cannibalism and aggressive tion, these EE structures seemed to improve improve the psychological and physiolog- [7]. In this way, the addition of EE in captive ferent colours can lead to different effects Another aspect to consider is that the intro- behaviour in the rearing environment [11] predatory avoidance, a relevant aspect for ical wellbeing of animals in captivity, pro- fishes might help fishes to cope better with [33] [34] [35]. duction of new objects in the environment [12] [13]. Other studies showed that EE successful restocking programmes [47]. viding new sensorial and motor stimulation such stressful events. can cause negative mental states (‘neo- structures, such as plastic tubes and shred- Other EE structures can provide incuba- Other studies on Gilthead seabream add- in order to help meet their behavioural and phobia’) in some fishes, or an increase of In recent years there has been an increase ding, can in addition reduce fin damage tion substrate. Salmonid alevins (yolk-sac ed hanging plant-fibre ropes in rearing en- psychological needs, and increase the ani- territoriality and aggressive/defensive at- of interest on the effects of EE in captive and erosion, and decrease related fin in- fry) hatch from eggs buried in gravel and vironments (tanks and cages), showing that mal’s behavioural and animal skills options, tacks [51] [52] [53]. fishes of farming interest, and therefore in fections, on 3 species of salmonids [14] spend the first part of their life within this such simple structures can reduce fin ero- while reducing the frequency of abnormal the number of related studies. Depending [15] [16] [17] [18], but also reduce the substrate. Adding hatching mats at the bot- sions, modify distribution of fishes, increase In addition, structural EE can be imple- behaviours. on the objective, the enrichment can be (1) swimming activity and net-interactions on tom of the tanks provides a wide range of spatial use and exploration, as well as fish mented together with other kinds of EE, For those reasons, the addition of struc- physical if it is an added structure or any Atlantic cod (Gadus morhua) [19] [20] positive effects, which are already widely cognitive and learning abilities [48] [49] such as sensorial (e. g. wall and bottom tures to enrich the rearing environment modification; (2) sensorial by which the [21] [22]. The implementation of EE struc- demonstrated on different salmonids spe- [50] (see figure 1). Nevertheless, there are colours, lights, covers, and noise), occu- (structural EE) is considered as a highly rec- sensory organs are stimulated; (3) occu- tures can also affect fish territoriality, and cies (for a review see [10]). These hatch- many other studies in scientific literature that pational (e. g. water flow currents and ommended tool to guarantee or improve pational when the possibilities for exercise some studies with Cichlids and plastic sea- ing mats improve growth and survival of show contradictory, undesired or unexpect- disturbances), social (e. g. densities or the welfare of laboratory or captive fishes or psychological challenge are given; (4) weed mimics demonstrated that such effects alevines, reduce yolk‐sac constrictions and ed results [10], which might indicate the space available, presence of other spe- [5], and may therefore be an effective way dietary which includes changes in the type are highly density-dependent [23][24]. improve yolk conversion efficiency, reduce use of inadequate structures (wrong design cies) and dietary (e. g. food type or to promote positive welfare in captivity [6]. or the delivery of food; and (5) social if alevines swimming activity and malforma- or materials) for each specific species, life- feeding strategy) aspects. Therefore, the There are different materials that can be However, very few fish farming companies any type of contact with conspecifics and/ tions, and permit rest in the normal position stage and rearing conditions. effect of the EE on fish welfare is not al- added to the rearing environment provid- apply this type of tool in their facilities to- or other species is allowed. The following at the bottom. It has been shown that they ways clear because the reaction can be ing floor substrate (e. g. sand, pebbles, day, and some enrichment strategies might lines are focused on the first type, structural also promote positive physiological chang- Other considerations different depending on the species, the cobbles, stones, etc.). Some studies on sal- not work in the intended way. This might EE, given that it is probably the best known es, increase brain growth, decrease stress, and remarks life-stage, the number of fishes affected, monids (Oncorhynchus clarkii, O. mykiss) the husbandry system, and the type of the probably be due to the poor communica- among EE measurements, and therefore the activity and oxygen consumption. Indeed, Overall, it has been shown that EE influ- demonstrated that adding such kind of enrichment [54] [55]. It is necessary there- tion between researchers and producers, most used from labs to farms nowadays. several commercial salmon hatching mats ences several aspects of the biology and

40 I FROM THE RESEARCH I 41 FROM THE RESEARCH

fore to take into account all these aspects References longifilis élevés en cage flottante.Belgian [22] Zimmermann E W, Purchase C F, and [32] Kang D Y and Kim H C, 2013. Impor- [41] Crank K M, Kientz J L, and Barnes before designing and using any EE at [1] Smith C P, Taylor V, and Nicol C, journal of zoology, 137(2), 157. Fleming I A, 2012. Reducing the incidence tance of bottom type and background color M E, 2019a. An evaluation of vertically farms, as well as to expand the knowledge of net cage biting and the expression of for growth and blindside hypermelanosis of suspended environmental enrichment struc- 1995. Environmental Enrichment Informa- [13] Slavík O, Maciak M, and Horký P, of the effects of EE and its applicability in escaperelated behaviors in Atlantic cod the olive flounder, Paralichthys olivaceus. tures during Rainbow Trout rearing. North tion Resources for Laboratory Animals, 2012. Shelter use of familiar and unfamiliar the aquaculture industry in a wider extent, (Gadus morhua) with feeding and cage Aquacultural Engineering, 57, 1–8. American Journal of Aquaculture, 81(1), 1965–1995: Birds, Cats, Dogs, Farm Ani- groups of juvenile European catfish Silurus adapting EE solutions to the biology of the enrichment. Applied animal behaviour 94–100. mals, Ferrets, Rabbits, and Rodents (No. 2). glanis. Applied Animal Behaviour Science, [33] Batzina A and Karakatsouli N, 2012. species and the farming systems. science, 141(1–2), 71–78. DIANE Publishing. 142(1–2), 116–123. The presence of substrate as a means of [42] Huysman N, Krebs E, Voorhees J M, [23] Barley A J and Coleman R M, 2010. environmental enrichment in intensively and Barnes M E, 2019. Use of Two Verti- [2] Newberry R C, 1995. Environmental [14] Bosakowski T and Wagner E J, 1995. Take Home Message Habitat structure directly affects aggres- reared gilthead seabream Sparus aurata: cally-Suspended Environmental Enrichment enrichment: increasing the biological rel- Experimental use of cobble substrates in sion in convict cichlids Archocentrus nigro- growth and behavioral effects. Aquacul- Arrays during Rainbow Trout Rearing in Cir- evance of captive environments. Applied concrete raceways for improving fin condi- fasciatus. Current Zoology, 56(1), 52–56. ture, 370, 54–60. cular Tanks. International Journal of Innova- Structural environmental enrichment Animal Behaviour Science, 44(2–4), tion of cutthroat (Oncorhynchus clarki) and tive Studies in Aquatic Biology and Fisheries, is considered a highly recommended 229–243. rainbow trout (O. mykiss). Aquaculture, [24] Torrezani C S, Pinho-Neto C F, Miyai [34] Batzina A, Dalla C, Papadopoulou- strategy to guarantee or improve the 5, 25–30. [3] Mellen J and Sevenich MacPhee M, 130(2–3), 159–165. C A, Sanches F H C, and Barreto R E, Daifoti Z, and Karakatsouli N, 2014a. welfare of laboratory or captive fish- 2013. Structural enrichment reduces ag- Effects of environmental enrichment [43] Jones M D, Krebs E, Huysman N, 2001. Philosophy of environmental enrich- [15] Wagner E J, Ross D A, Routledge es. Its objective is to improve the psy- gression in Tilapia rendalli. Marine and on growth, aggressive behaviour and Voorhees J M, and Barnes M E, 2019. ment: past, present, and future. Zoo Biolo- D, Scheer B, and Bosakowski T, 1995. chological and physiological wellbe- freshwater behaviour and physiology, brain monoamines of gilthead sea- Rearing Performance of Atlantic Salmon gy, 20(3), 211–226. Performance and behavior of cutthroat trout ing of animals in captivity, providing 46(3), 183–190. bream Sparus aurata reared under dif- Grown in Circular Tanks with Vertically-Sus- (Oncorhynchus clarki) reared in covered new sensorial and motor stimulation [4] Shepherdson D J, 2003. Environmental ferent social conditions. Comparative pended Environmental Enrichment. Open raceways or demand fed. Aquaculture, [25] Wagner E J, Routledge M D, and in order to help meet their behav- enrichment: past, present and future. Inter- Biochemistry and Physiology Part A: Mo- Journal of Animal Sciences, 9(02), 249. 136(1–2), 131–140. Intelmann S S, 1996. Fin condition and ioural and psychological needs, and national Zoo Yearbook, 38(1), 118–124. lecular & Integrative Physiology, 169, health profiles of albino rainbow trout [44] Muggli A M, Barnes J M, and Barnes, increase the behavioural and animal [16] Arndt R E, Routledge M D, Wagner 25–32. [5] Brydges N M and Braithwaite V A, reared in concrete raceways with and with- M E, 2018. Vertically-Suspended Environ- skills options of the animals, while E J, and Mellenthin R F, 2001. Influence 2009. Does environmental enrichment out a cobble substrate. The Progressive fish- [35] Batzina A, Kalogiannis D, Dalla C, mental Enrichment Alters the Velocity Pro- reducing the frequency of abnormal of raceway substrate and design on fin affect the behaviour of fish commonly culturist, 58(1), 38–42. Papadopoulou-Daifoti Z, Chadio S, and files of Circular Fish Rearing Tanks.World behaviours. In fish farms, the environ- erosion and hatchery performance of used in laboratory work? Applied Animal Karakatsouli N, 2014c. Blue substrate Journal of Engineering and Technology, ments where the fishes are kept gen- rainbow trout. North American Journal of [26] McVicar A H, 1987. Black patch ne- Behaviour Science, 118(3–4), 137–143. modifies the time course of stress response 7(1), 208–226. erally lack structures, mainly for prac- Aquaculture, 63(4), 312–320. crosis of the skin of Solea solea (L.): the in gilthead seabream Sparus aurata. Aqua- tical reasons for the farmer. However, [6] Fife-Cook I and Franks B, 2019. Posi- role of sand in prophylaxis and treatment. [45] Rosburg A J, Fletcher B L, Barnes, [17] Berejikian B A, 2005. Rearing in culture, 420, 247–253. during a cycle of aquaculture produc- tive welfare for fishes: rationale and areas Journal of Fish Diseases 10, 59–63. M E, Treft C E, and Bursell B R, 2019. Verti- enriched hatchery tanks improves dorsal tion there are several situations that for future study. Fishes, 4(2), 31. [36] Gessner J, Kamerichs C M, Kloas W, cally-Suspended Environmental Enrichment fin quality of juvenile steelhead. North [27] McVicar A H and White P G, 1982. can be very stressful for fishes, and and Wuertz S, 2009. Behavioural and Structures Improve the Growth of Juvenile [7] Ashley P J, 2007. Fish welfare: cur- American Journal of Aquaculture, 67(4), The prevention and cure of an infectious structural enrichment might help im- physiological responses in early life phases Landlocked Fall Chinook Salmon. Inter- rent issues in aquaculture. Applied Animal 289–293. disease in cultivated juvenile Dover prove the welfare of fishes, especially of Atlantic sturgeon (Acipenser oxyrinchus national Journal of Innovative Studies in Behaviour Science, 104(3–4), 199–235. sole, Solea solea (L.). Aquaculture 26, after stressful activities. In recent years [18] Näslund J, Rosengren M, Del Vil- Mitchill 1815) towards different substrates. Aquatic Biology and Fisheries, 5, 17–24. 213–222. there has been an increase of interest [8] Conte F S, 2004. Stress and the welfare lar D, Gansel L, Norrgård J R, Persson Journal of applied Ichthyology, 25, 83–90. [46] White S C, Krebs E, Huysman N, on the effects of structural enrichment of cultured fish. Applied Animal Behaviour L, and Kvingedal E, 2013. Hatchery tank [28] Ottesen O H, Noga E J, and Sandaa [37] Wiszniewski G, Duda A, and Kolman Voorhees J M, and Barnes M E, 2019. Use in captive fishes, and therefore in the Science, 86(3–4), 205–223. enrichment affects cortisol levels and shel- W, 2007. Effect of substrate on progression R, 2010. Wplyw warunkow przet-rzymy- of suspended plastic conduit arrays during number of related studies, though ter-seeking in Atlantic salmon (Salmo salar). and healing of skin erosions and epider- [9] Galhardo L and Oliveira R F, 2009. wania larw jesiotra ostroosego na ich wz- Brown Trout and Rainbow Trout rearing in there are still some gaps to bridge. Canadian Journal of Fisheries and Aquatic mal papillomas of Atlantic halibut, Hippo- Psychological stress and welfare in fish. rost i przezywalnosc. Komunikaty Rybackie, circular tanks. North American Journal of Sciences, 70(4), 585–590. glossus hippoglossus (L.). Journal of fish Annual Review of Biomedical Sciences, 2, 8–10. Aquaculture, 81(1), 101–106. diseases, 30(1), 43–53. 1–20. [19] Salvanes A G V and Braithwaite V A, [38] Boucher M A, McAdam S O, and [47] Crank K M, Voorhees J M, and 2005. Exposure to variable spatial informa- [29] Ottesen O H and Strand H K, 1996. [10] Näslund J and Johnsson J I, 2016. Shrimpton J M, 2014. The effect of temper- Barnes M E, 2019b. Predator avoidance tion in the early rearing environment gen- Growth, development, and skin abnormali- Environmental enrichment for fish in captive ature and substrate on the growth, develop- of rainbow trout reared with environmental erates asymmetries in social interactions in ties of halibut (Hippoglossus hippoglossus environments: effects of physical structures ment and survival of larval white sturgeon. enrichment. Journal of Fisheries and Aqua- cod (Gadus morhua). Behavioral Ecology L.) juveniles kept on different bottom sub- and substrates. Fish and Fisheries, 17(1), Aquaculture, 430, 139–148. culture Development. 1–30. and Sociobiology, 59(2), 250. strates. Aquaculture, 146(1–2), 17–25. [39] Kientz J L and Barnes M E, 2016. [48] Arechavala-Lopez P, Diaz-Gil C, [20] Salvanes A G, Moberg O & Braith- [30] Dou S, Seikai T, and Tsukamoto K, [11] Hossain M A, Beveridge M C, and Structural complexity improves the rearing Saraiva J L, Moranta D, Castanheira M F, waite V A, 2007. Effects of early experi- 2000. Cannibalism in Japanese flounder Haylor G S, 1998. The effects of density, performance of rainbow trout in circular Nuñez-Velázquez S, and Grau A, 2019. ence on group behaviour in fish.Animal juveniles, Paralichthys olivaceus, reared light and shelter on the growth and sur- tanks. North American journal of aqua- Effects of structural environmental enrich- Behaviour, 74(4), 805–811. under controlled conditions. Aquaculture, vival of African catfish (Clarias gariepinus culture, 78(3), 203–207. ment on welfare of juvenile seabream 182(1–2), 149–159. Burchell, 1822) fingerlings.Aquaculture, [21] Moberg O, Braithwaite V A, Jensen (Sparus aurata). Aquaculture Reports, 15, [40] Kientz J L, Crank K M, and Barnes 160(3–4), 251–258. K H, and Salvanes A G V, 2011. Effects of [31] Kang D Y and Kim, H C, 2012. 100224. M E, 2018. Enrichment of circular tanks habitat enrichment and food availability on Relevance of environmental factors and [12] Coulibaly A, Koné T, Ouattara N I, with vertically suspended strings of colored [49] Arechavala-Lopez P, Caballero- the foraging behaviour of juvenile Atlantic physiological pigment hormones to blind- N Douba V, Snoeks J, Kouamélan E P, and balls improves rainbow trout rearing perfor- Froilán J C, Sureda A, Jiménez M, Sara- Cod (Gadus morhua L). Environmental side hypermelanosis in the cultured flounder, Bi G G, 2007. Évaluation de l‘effet d‘un mance. North American Journal of Aqua- iva J L, and Moranta D, 2020. Enriched biology of fishes,91(4), 449–457. Paralichthys olivaceus. Aquaculture, 356, système de refuge sur la survie et la crois- culture, 80(2), 162–167. environments enhance cognition, explora- 14–21. sance des alevins de Heterobranchus tory behaviour and brain physiological

42 I FROM THE RESEARCH I 43 FROM THE RESEARCH FROM THE RESEARCH

functions of Sparus aurata. Scientific water is treated and gets re-used ([2], 31). When it comes to optimising conditions, Reports, 10: 11252. doi: 10.1038/ Knowledge as prerequi- p. 20). the idea is to find a balance between costs s41598-020-68306-6. and benefits. This may lead to not recommen- site for fish welfare — Important for the construction are often prac- ding the condition with highest potential for [50] Muñoz L, Aspillaga E, Palmer M, FishEthoBase as a basis tical considerations behind which the wel- growth but the one with highest promise for Saraiva J L, and Arechavala-Lopez P, fare of the fishes takes a back seat: in the overall profit [12] [13] [14]. 2020. Acoustic telemetry as potential tool Jenny Volstorf (Dr.) Asian region, one uses rice fields or pits that to monitor fish swimming behaviour in sea- result from digging soil [3] [4] — yet missing Furthermore, whether an individual is well, Editor-in-chief FishEthoBase, cage aquaculture. Frontiers in Marine Sci- protection from rain, heat, and predators is only partly evident from the growth rate. Fish Ethology and Welfare Group, ence, doi: 10.3389/fmars.2020.00645 may afflict the fishes[5] . Concrete tanks Without a doubt, health is an important Centro de Ciencias do Mar (CCMAR), are an option to keep fishes in regions that prerequisite for high welfare. Fishes, how- [51] Castanheira M F, Herrera M, Cos- Rua José Mateus Horta 3, do not offer enough soil — yet, having no ever, are also sentient [15] and intelligent tas B, Conceição L E, and Martins C I, 38000-536 Faro, Portugal substrate at all may lead to fin erosion[6] , beings [16] [17] — ethics demand these 2013. Can we predict personality in fish? [email protected] and the water quality may be worse than needs be respected. Instead of pursuing just Searching for consistency over time and in earthen ponds [7] [8]. Cages make a health-based functional approach, one across contexts. PLoS One, 8(4), e62037. Change of focus from profitability use of the naturally occurring conditions of could combine it with a nature-based and to welfare [52] Castanheira M F, Conceição L E, open waters — nevertheless, being exposed feelings-based approach [18]. Millot S, Rey S, Bégout M L, DamsgAard Since 1950, the production in aquaculture to storms, algal bloom, temperature, and To achieve that, it takes building a habitat B, and Martins C I, 2017. Coping styles in has increased from 0.6 million to 82.1 predators may result in stress [9]. Recirculat- and conditions which resemble those of the farmed fish: consequences for aquaculture. million tonnes per year, with a tendency ing Aquaculture Systems score with the pos- original surrounding as best as possible and Reviews in Aquaculture, 9(1), 23–41. to rise [1]. This comprises inland as well sibility to optimally control water parameters allowing natural behaviour (nature-based as marine aquaculture, with inland aqua- [10] — but the accumulation of substances [53] Woodward M A, Winder L A, and approach), meaning the fish are free from culture being the larger part at 47 million may hinder growth [11]. If fish welfare is Watt P J, 2019. Enrichment increases hunger, thirst, discomfort, pain, fear, and tonnes. The range of systems is large. In of second concern after practicability, the aggression in zebrafish. Fishes, 4(1), 22. stress, providing positive experiences as Asia, which by far leads the aquaculture efforts to implement it will reach a limit. For well as cognitive challenges, and consid- [54] Sullivan M, Lawrence C, and Blache sector worldwide (almost 96 % of aqua- a species-appropriate housing, the system ering social structures and differences in D, 2016. Why did the fish cross the tank? culture employees worldwide are from should be adjusted to the animal, not the personality (feelings-based approach [18] Objectively measuring the value of en- Asia; China produces more farmed fish other way around. richment for captive fish.Applied Animal than the rest of the world combined ([2], [19] [20]). To be able to do so, habitat, Behaviour Science, 174, 181–188. p. 5 and 28), earthen ponds dominate. Of course growth and mortality are che- conditions, and prerequisites for positive ex- Furthermore, there are raceways, tanks, cked — but against the background of maxi- periences and welfare have to be known. [55] Toni M, Manciocco A, Angiulli E, Al- cages, and Recirculating Aquaculture mising profits. Aquaculture is a business that The amount of considerations and experi- leva E, Cioni C, and Malavasi S, 2019. As- Systems which are systems in which the millions of people worldwide live on ([2], p. mental studies on that increases constantly. sessing fish welfare in research and aqua- culture, with a focus on European directives. animal, 13(1), 161–170. [56] Galhardo L, Almeida O & Oliveira R F, 2009. Preference for the presence of substrate in male cichlid fish: effects of social dominance and context. Applied Animal Behaviour Science, 120(3-4), 224–230. [57] Batzina A, Dalla C, Tsopelakos A, Papadopoulou-Daifoti Z, and Kar- akat-souli N, 2014b. Environmental enrich- ment induces changes in brain monoamine levels in gilthead seabream Sparus aurata. Physiology & behavior, 130, 85–90.

Figure 1: Examples of different aquaculture systems, clockwise: earthen pond without protection from heat and rain, from [23]; concrete tank without substrate, from [23]; recirculation system with circulation pump, from [27]; floating net cage, from [27].

44 I FROM THE RESEARCH I 45 FROM THE RESEARCH

Knowledge as prerequisite the African catfish (Clarias gariepinus) on Ethological short profiles for welfare inundated vegetation as well as mud, the and FishEthoScore Category Sub-category general statement on substrate preference Our team from the Fish Ethology and Wel- For a faster overview, the FishEthoBase pre- 10. Growth 10.1 Ontogenetic development fare Group and fair-fish international re- is opportunistic [23]. In a separate part of sents a short profile with 10 selected criteria 10.2 Sexual conversion spectively has declared it our task to gather the FishEthoBase, we convert the findings for each species. For each age class sep- and provide open access to all ethological from the 19 categories into specific recom- arately, we compare the findings from the 10.3 Sex ratio knowledge of the most commonly farmed mendations for farmers. For substrate, this wild with the situation in aquaculture and 10.4 Effects on growth could be: ‘For the most natural solution, fish species in the FishEthoBase — as a stim- estimate the probability for welfare under 10.5 Deformities and malformations ulation to extend existing aquaculture sys- provide mud and vegetation’ [24]. The minimal conditions (‘Likelihood’) and un- 11. Reproduction 11.1 Nest building tems and as enrichment for the planning of recommendations are not meant to be an der high-standard conditions (‘Potential’) new systems but also to point to knowledge all-including rearing manual but rather hints as well as how certain we are of these 11.2 Attraction, courtship, mating gaps [21]. Our goal is that fishes in captiv- at which conditions are disadvantageous to judgements given quantity and quality of 11.3 Spawning welfare. The three parts — introductory over- ity experience high welfare and may reach the references (‘Certainty’). Whenever we 11.4 Fecundity their full potential [22]. view, findings, recommendations — form the score ‘high’ in a criterion, the counter of the 11.5 Brood care, breeding ethological full profile of a species. At the three-component FishEthoScore increases In 19 categories and several sub-catego- moment, FishEthoBase offers 11 full profiles (Likelihood, Potential, Certainty), at most 12. Senses 12.1 Vision ries (Table 1), we present the essences of (as of August 2020). resulting in 10|10|10 with 10 criteria. At 12.2 Olfaction (and taste, if present) studies individually for each species and currently 46 short profiles(as of August summarise several studies in a general state- 12.3 Hearing 2020), the Nile Tilapia (Oreochromis nilot- ment. If, for example, there are findings for 12.4 Touch, mechanical sensing icus) with a FishEthoScore of 3|8|6 has the 12.5 Lateral line

Table 1: Findings categories and sub-categories of a full profile in the FishEthoBase. 12.6 Electrical sensing 12.7 Nociception, pain sensing Category Sub-category 12.8 Other

1. Remarks 1.1 General remarks 13. Communication 13.1 Visual 1.2 Other remarks 13.2 Chemical 2. Ethograms 13.3 Acoustic 3. Distribution 13.4 Mechanical 4. Natural co-existence 13.5 Electrical 5. Substrate and/or shelter* 5.1 Substrate 13.6 Other 5.2 Shelter or cover 14. Social behaviour 14.1 Spatial organisation 6. Food, foraging, hunting, feeding 6.1 Trophic level and general considerations on food needs 14.2 Social organisation 6.2 Food items 14.3 Exploitation 6.3 Feeding behaviour 14.4 Facilitation 7. Photoperiod 7.1 Daily rhythm 14.5 Aggression 7.2 Light intensity 14.6 Territoriality 7.3 Light colour 15. Cognitive abilities 15.1 Learning 8. Water parameters 8.1 Water temperature 15.2 Memory 8.2 Oxygen 15.3 Problem solving, creativity, planning, intelligence 8.3 Salinity 15.4 Other 8.4 pH 16. Personality, coping styles 8.5 Turbidity 17. Emotion-like states 17.1 Joy 8.6 Water hardness 17.2 Relaxation 8.7 NO4 17.3 Sadness 8.8 Other 17.4 Fear 9. Swimming 9.1 Swimming type, swimming mode 18. Self-concept, self-recognition 9.2 Swimming speed 19. Reactions to husbandry 19.1 Stereotypical and vacuum activities 9.3 Home range 19.2 Acute stress 9.4 Depth 19.3 Chronic stress 9.5 Migration 19.4 Stunning reactions

* Highlighted categories are also dealt with in the short profile. * Highlighted categories are also dealt with in the short profile.

46 I FROM THE RESEARCH I 47 FROM THE RESEARCH

best prospect to experience high welfare b) determine connections between natural with a broad spectrum of indicators for wel- Fish welfare in aquaculture. The second best FishEtho- conditions and behaviour, e. g., triggers for fare [20] [27] [30] (Table 2). This allows us Example from the FishEthoBase indicator Score of 0|6|5 holds the African catfish reproduction or migration. to give extensive advice in the recommen- (C. gariepinus). The majority (39 species) dations part for farmers. Behaviour reaches a potential of 2 max. 3. Knowledge of behaviour in General recommendations — albeit exten- Ventilatory Nile tilapia adults (O. niloticus) displayed increased ventilatory frequency when paired captivity (aquaculture or lab) to Even though the FishEthoBase momentarily sive and species specific — reach a limit frequency with a larger resident [44] covers just a fraction of the more than 530 a) determine plasticity, e. g., higher temper- in the face of differences in farming con- Crit. 14.2 Social organisation —› Features of subordination aquatic species currently farmed worldwide ature or higher density than in the wild, ditions, personalities, and changes over or after 30 min confinement[45] Crit. 19.2 Acute stress —› Confinement (among them 362 fin fishes and a further b) adjust conditions for which there is no time. Ideal would be the implementation 68 aquatic vertebrates [2]), the mostly low model in the wild, e. g., stress reactions to depending on the respective farming pop- Rainbow trout juveniles (Oncorhynchus mykiss) displayed higher opercular beat rate after injection FishEthoScore is disillusioning. Among the stunning and slaughter. ulation and — even better — depending on of acetic acid in upper and lower lips [46] reasons for the low score is missing know- the individuals. Technical innovations like Crit. 12.7 Nociception, pain sensing —› Nociception spectrum ledge. For the creation of short and full The knowledge of natural behaviour in the underwater video observations [31] and in- profiles we consult the following types of wild in particular is scarce. This is, how- dividual measuring tags [32] make a valu- Aggression African catfish fry (C. gariepinus) displayed more aggression with six knowledge: ever, the most important indicator for wel- able contribution. than three feeding times per day [47] fare [26]. How is a fish farmer supposed Crit. 6.3 Feeding behaviour —› Feeding frequency and stress All efforts to avoid stress and stress-releasing 1. Knowledge of natural to know whether a fish displays stress, if African catfish juvenilesdisplayed more chasing, bites, barbel fights factors do not necessarily lead to the goal under 24 h than 12 h photoperiod [48] behaviour in the wild to one is not able to distinguish relaxed from stressed behaviour? Besides avoidance of of creating high welfare — a life without Crit. 7.1 Daily rhythm —› Photoperiod and stress a) build aquaculture systems accordingly stress, natural behaviour provides insights sorrows but also without positive experien- and thereby promote natural behaviour, Atlantic salmon parr (S. salar) displayed more aggression under 1 lux than in darkness [49] into what the ideal state should look like. As ces is a boring life [30]. Which stimuli are e. g., natural reproductive behaviour deter- Crit. 7.1 Daily rhythm —› Daily rhythm long as this state is not reached, a fish might perceived as positive can be determined mines substrate, stocking density, and sex with the help of preference tests [30]. Nile experience absence of stress at most but not Nile tilapia juveniles (O. niloticus) displayed more bites and lateral fights in aquaria with substrate ratio in captivity, Tilapia males (O. niloticus), for example, high welfare. For that to be the case, there than without [50] b) compare natural behaviour to that in aq- need to be positive incentives. More on that preferred gravel or shelter over bare bottom Crit. 5.1 Substrate —› Substrate and stress uaculture, recognise abnormal behaviour, later. when they had the choice [33]. Giving the and change conditions, e. g., higher fertil- individuals control can also have a positive Gilthead seabream juveniles (Sparus aurata) displayed more aggression than control individuals Observation of behaviour as the sole meth- ity in the wild could be an indication for effect: Carp juveniles (C. carpio), for ex- when they had experienced restraining before [51] od to determine welfare could fall short, sub-optimal conditions in captivity [25]. ample, displayed lower glucose or cortisol Crit. 15.1 Learning —› Learning and aggression though, because behaviour is variable levels if they triggered self-feeders as op- across time and differences in personality Swimming African catfish fry (C. gariepinus) displayed lower browsing and higher resting activity in aquaria 2. Knowledge of natural posed to being fed by hand [34]. A third with black plastic shade [52] [27]. Relying exclusively on physiological possibility are opportunities to explore and conditions in the wild to Crit. 5.2 Shelter or cover —› Shelter or cover and stress parameters is unreliable, too, because an discover the habitat — again, substrate and a) build aquaculture systems accordingly African catfish juveniles displayed more swimming and less resting activity under 24 h than 12 h increased cortisol level might as well hint other means of environmental enrichment and thereby promote natural behaviour, photoperiod and under 150 than 15 lux [48] at positive excitement instead of stress [28] play an important role [35]. The announce- e. g., photoperiod, temperature, and other Crit. 7.1 Daily rhythm —› Photoperiod and stress [29]. In the FishEthoBase, we cite studies ment of a reward and unexpected increase water parameters, Rainbow trout juveniles (O. mykiss) increased taking cover, decreased swimming in open area, increased ‘freezing’ when presented with skin extract from conspecifics[53] Crit. 13.2 Chemical —› Signalling stress Table 2: Fish welfare examples from the FishEthoBase. achieved higher relative critical swimming speed when fed 2 % or 1 % body weight than 0.5 % [54] Crit. 9.2 Swimming speed —› Swimming speed Fish welfare Example from the FishEthoBase displayed random and disorganised swimming under high rather than low stocking density [55] indicator Crit. 14.1 Spatial organisation —› Stocking density and stress Behaviour Atlantic salmon adults (S. salar) displayed erratic swimming and three times higher swimming speed Feeding African catfish juveniles (C. gariepinus), being transferred to an experimental aquarium, with infrasound [56] did not or barely feed in the first 24 h [40] Crit. 12.3 Hearing —› Noise and stress Crit. 16 Personality, coping styles —› Exploration-avoidance continuum Common carp juveniles (Cyprinus carpio) displayed erratic swimming European perch juveniles (Perca fluviatilis) displayed lower feed intake with husbandry disturbance when sound was switched on [57] than in undisturbed tanks [41] Crit. 12.3 Hearing —› Noise and stress Crit. 19.3 Chronic stress —› Husbandry disturbance Pangasius juveniles (Pangasianodon hypophthalmus) swam faster in green aquaria Atlantic salmon juveniles (Salmo salar) displayed higher feed intake in isolation than in group rearing, than in white ones [58] probably due to absent food competition [42] Crit. 9.2 Swimming speed —› Swimming speed Crit. 6.3 Feeding behaviour —› Food competition and growth Stereotypical African catfish juveniles(C. gariepinus) increased air breathing with increasing stocking density [59] European seabass juveniles (Dicentrarchus labrax) maintained the subdivision in zero-trigger-, and abnormal Crit. 14.1 Spatial organisation —› Stocking density and stress low-trigger and high-trigger individuals with the self-feeder even after size grading and disruption behaviour of social structure [43] Atlantic salmon adults (S. salar) jumped 18 times more under high rather than under low light intensity [56] Crit. 14.2 Social organisation —› Social organisation type Crit. 12.1 Vision —› Visible spectrum

48 I FROM THE RESEARCH I 49 FROM THE RESEARCH

Fish welfare Fish welfare Example from the FishEthoBase Example from the FishEthoBase indicator indicator

Rainbow trout juveniles (O. mykiss) took longer to go near a novel rather than a known object, Health spent less time in its vicinity, more out of reach [15] Injuries Crit. 16. Personality, coping styles —› Exploration-avoidance continuum Rainbow trout fry (O. mykiss) had less fin erosion in tanks with substrate than those without[6] Exploratory Crit. 5.1 Substrate —› Substrate and stress behaviour Common carp juveniles (C. carpio) differed in the time they needed to leave cover to explore a novel surrounding; the differences were consistent over weeks [60] [61] Nile tilapia juveniles (O. niloticus) displayed injuries under 24 h scotoperiod [74] Crit. 16. Personality, coping styles —› Exploration-avoidance continuum Crit. 7.1 Daily rhythm —› Photoperiod and growth

Atlantic salmon parr (S. salar) displayed more aggression and more attacks under predicted Immune reactions Pacific whiteleg shrimp juveniles (L. vannamei) displayed increased haemocyte levels after confinement Food-anticipatory rather than unpredicted feeding schedule [62] and air exposure [75] behaviour Crit. 6.3 Feeding behaviour —› Feed delivery and stress Crit. 19.2 Acute stress —› Confinement

Pain Pacific whiteleg shrimp adult females (Litopenaeus vannamei) rebound when having Pangasius juveniles (P. hypophthalmus) displayed higher levels of immunoglobulin when given their eyestalk ablated without anaesthesia, displayed erratic spiral swimming [63] levamisole rather than lipopolysaccharide or saline [76] Crit. 12.7 Nociception, pain sensing —› Nociception spectrum Crit. 6.2 Food items —› Feed enrichment and stress tolerance

Rainbow trout juveniles (O. mykiss) increased taking cover, rocked from side to side, Common carp fry (C. carpio) had higher levels of leucocytes, gut bacteria, and lactic acid bacteria given and rubbed their lips on the substrate or the aquarium wall after being injected food enriched with 2-3% fructo-oligosaccharides [77] with acid in the lips [46] Crit. 6.2 Food items —› Feed enrichment and stress tolerance Crit. 12.7 Nociception, pain sensing —› Nociception spectrum Note: Indicators from [20] [27] [30]. Fear Rainbow trout juveniles (O. mykiss) learned to swim to another compartment when an object plunged into the aquarium, some ‘'froze'’ and sank to the bottom [64] Crit. 17.4 Fear of the reward may lead to positive experi- Nature is not necessarily ideal in yet anoth- species to experience high welfare under Common carp juveniles (C. carpio) could not be tested in isolation from the group because ences [28]. An example of positive emo- er way: a species is adapted to the con- high-standard aquaculture conditions ac- they displayed such strong indications of stress, e. g., restlessness [65] tions while expecting a reward are cods ditions of its ecological niche, but water cording to the FishEthoScore [21]. Even Crit. 17.4 Fear (Gadus morhua) that gather at the feeding temperatures for example display a certain if we assume that domestication removes site in anticipation of food [36]. range given season or other external fac- from the species-specific natural behaviour, Nile tilapia juveniles (O. niloticus), having escaped faster from a confinement situation, tors. Temperatures at the upper limit of the it takes further research to find hints that na- returned slower to the area and spent less time there than other juveniles [66] Criticism on nature range usually result in higher growth (see ture becomes redundant as a yardstick as Crit. 17.4 Fear as yardstick for welfare criteria 8.1.1 Standard temperature range domestication progresses. Playing and 8.1.3 Temperature and growth in the Rainbow trout kelts (O. mykiss) dashed at coins that were thrown into the water – play? [67] The last example already showed that nature Until then, we from the Fish Ethology and full profiles of the FishEthoBase). Aquacul- Crit. 15.4 Other —› Playing does not have to be the model in all cases. Welfare Group advocate focusing on farm- ture allows the water parameters to be con- Migration in search of feed is no longer nec- ing a small number of species whose needs Pacific whiteleg shrimp adult males (L. vannamei) approached other males or immature females, trolled and therefore results in potentially essary for farmed fishes fed regularly and are well researched and easily satisfiable in crawled underneath their tail, chased them – playing? [68] better growth than in the wild. Thus, spe- sufficiently. Also, migration due to changing captivity as well as with high plasticity and Crit. 15.4 Other —› Playing cies may profit from conditions in aquacul- water parameters or mating migration do low tendency for stress. The short profiles not play a role in aquaculture — this is at ture even if they are not a realistic image of Preferences Nile tilapia adult males (O. niloticus) preferred sand over sand-bivalve-mixture for nest building, of the FishEthoBase allow an evaluation of the natural water conditions including oscil- avoided stones and barren aquaria [69] least what is assumed. Whether the need to the suitability for aquaculture by means of lations throughout the year. The transition to Crit. 11.1 Nest building migrate is non-existent due to missing ne- the FishEthoScore [39]. Only with sufficient stress is fluid, though, and further research cessity is just as unclear as whether not be- knowledge and further research will it be is needed — especially preference tests — to Communication African catfish juveniles (C. gariepinus) elicited an electrical discharge ing able to pursue the need is experienced possible to provide fish species in captivity during aggressive encounters with conspecifics [70] find the ideal temperature range. as loss of welfare [26] [37]. It is difficult with conditions that closely resemble those Crit. 13.5 Electrical —› Signalling stress to distinguish external triggers (e. g., chang- The third aspect that could be argued about in nature or that individuals prefer respec- ing water level or temperature) from internal Nile tilapia adult males (O. niloticus) elicited a number of sounds why nature is not the gold standard results tively. This knowledge is gathered better, causes. Here again, more knowledge of when a rival entered their territory [71] from domestication and the associated ad- faster, and with more detail for a manage- Crit. 13.3 Acoustic —› Sounds during nest defence the ethology of a species is a prerequisite justment to aquaculture conditions. There is able number of farmed fish species. to provide high welfare. Indications to solve no survival stress in the face of predators Gilthead seabream juveniles and adults (S. aurata) turned to darker body colouration the conflict or realise that there is no con- or lack of feed; individuals do not have and erected their dorsal fin during aggressive encounters[72][73] flict after all, because the plasticity of the to compete for mating partners; it is not Crit. 13.1 Visual —› Signalling aggression individuals is large enough, can only come so much the risk-avoiding but the stress-re- from further research — for example by sistant personality type that is in demand. Pangasius juveniles (P. hypophthalmus) turned to darker body colouration in green and black studies investigating what individuals are than white tanks [58] Fish farming, however, does not have the willing to do to satisfy a need [26]. Crit. 13.1 Visual —› Colouration and habitat long tradition that farming terrestrial animals has [38], and the degree of domestication does not correlate with the potential of a

50 I FROM THE RESEARCH I 51 FROM THE RESEARCH

References [9] Maricchiolo G, Mirto S, Caruso G, Ca- [15] Sneddon L U, Braithwaite V A, wild white shrimp males Litopenaeus van- https://doi.org/10.1016/j.aquae- Take Home Message [1] FAO, 2020. The State of World Fish- ruso T, Bonaventura R, Celi M, Matranga and Gentle M J, 2003. Novel object namei (Decapoda: Penaeidae). Internatio- ng.2016.03.002. V, and Genovese L, 2011. Welfare status test: examining nociception and fear in nal Journal of Tropical Biology and Conser- eries and Aquaculture 2016. Contributing [33] Delicio H C, Bareto R E, Normandes • Often, when building aquaculture of cage farmed European sea bass (Dicen- the rainbow trout. The Journal of Pain 4: vation 55. https://doi.org/10.15517/ to food security and nutrition for all. Rome: E B, Luchiari A C, and Marcondes A L, systems, the focus lies on practica- trarchus labrax): A comparison between sub- 431–440. https://doi.org/10.1067/ rbt.v55i1.6071 — see also the FishEth- FAO. 2006. A place preference test in the fish bility, when deciding about condi- merged and surface cages. Aquaculture 314: S1526-5900(03)00717-X — see also oBase profile of Litopenaeus vannamei: Nile tilapia. Journal of Experimental Ani- tions, the focus lies on profitability. [2] FAO, 2016. The State of World Fish- 173–181. https://doi.org/10.1016/ Lynne Sneddon’s contribution on ‘Sentience http://fishethobase.net/db/21/ mal Science 43: 141–148. https://doi. eries and Aquaculture 2016. Contributing j.aquaculture.2011.02.001 — see also in Fishes’ in this issue. • Fishes are sentient and intelligent [26] Bracke M B M and Hopster H, 2006. org/10.1016/j.jeas.2006.01.001 — to food security and nutrition for all. Rome: the FishEthoBase profile of von Dicentrarchus and deserve having their needs [16] Bernardi G, 2012. The use of tools by Assessing the Importance of Natural Behav- see also the FishEthoBase profile of O. nilo- FAO. labrax: http://fishethobase.net/db/14/) satisfied. wrasses (Labridae). Coral Reefs 31: 39–39. ior for Animal Welfare. Journal of Agricul- ticus: http://fishethobase.net/db/31/ [3] Edwards P, Little D C, and Yakupitiyage [10] Sturrock H, Newton R, Paffrath S, https://doi.org/10.1007/s00338-011- tural and Environmental Ethics 19: 77–89. • To do so, it takes knowledge of nat- [34] Klaren P H M, van Dalen S C M, A, 1997. A comparison of traditional and Bostock J, Muir J, Young J, Immink A, and 0823-6. https://doi.org/10.1007/s10806-005- ural conditions and natural behav- Atsma W, Spanings F A T, Hendriks J, and modified inland artisanal aquaculture sys- Dickson M, 2008. Prospective Analysis of 4493-7. iour, of prerequisites for positive [17] Brown C, 2015. Fish intelligence, Flik G, 2013. Voluntary timing of food in- tems. Aquaculture Research 28: 777–788. the Aquaculture Sector in the EU. PART 2: experiences and welfare. sentience and ethics. Animal Cognition [27] Martins C I M, Galhardo L, Noble take increases weight gain and reduces https://doi.org/10.1046/j.1365- Characterisation of Emerging Aquaculture 18: 1–17. https://doi.org/10.1007/ C, Damsgård B, Spedicato M T, Zupa W, basal plasma cortisol levels in common • The FishEthoBase aims to gather and 2109.1997.00942.x. Systems. Edited by Ilias Papatryfon. JRC s10071-014-0761-0 — see also Culum and Beauchaud M, et al, 2012. Behav- carp (Cyprinus carpio L.). Physiology & provide open access to all ethologi- Scientific and Technical Reports. European [4] Hambrey J, Edwards P, and Belton B, Brown’s and Cat Dorey’s contribution on ioural indicators of welfare in farmed fish. Behavior 122: 120–128. https://doi. cal knowledge of the most commonly Commission, Joint Research Centre, Insti- 2008. An ecosystem approach to fresh- ‘Pain and Emotion in Fishes’ in this issue. Fish Physiology and Biochemistry 38: 17– org/10.1016/j.physbeh.2013.08.020 farmed fish species. tute for Prospective Technological Studies. water aquaculture: a global review. In FAO 41. https://doi.org/10.1007/s10695- — cited in the FishEthoBase profile of [18] Fraser D, 2008. Understanding • To what extent aquaculture should Fisheries and Aquaculture Proceedings, [11] Martins C I M, Ochola D, Ende S S W, 011-9518-8. C. Carpio: http://fishethobase.net/ animal welfare. Acta Veterinaria Scandi- adhere to the natural habitat and 14:117–121. Rome, Italy: FAO. Eding Ep H, and Verreth J A J, 2009. Is db/12/. navica 50: S1. https://doi.org/10.1186/ [28] Boissy A, Manteuffel G, Jensen M B, natural conditions as a gold stand- growth retardation present in Nile tilapia [5] Kristanto A H, Slembrouck J, 1751-0147-50-S1-S1 — see also Joao Oppermann Moe R, Spruijt B, Keeling L J, [35] see Pablo Arechavala-Lopez’ contribu- ard or whether it may deviate from Oreochromis niloticus cultured in low wa- Subagja J, Pouil S, Arifin O Z, Prakoso Saraiva’s and Pablo Arechavala-Lopez’s and Winckler C, et al, 2007. Assessment tion on ‘Structural Enrichment’ in this issue. it without loss of fish welfare, further ter exchange recirculating aquaculture V A, and Legendre M, 2019. Survey on contribution ‘No longer the Elephant in the of positive emotions in animals to improve research needs to show. systems? Aquaculture 298: 43–50. [36] Nilsson J, Kristiansen T S, egg and fry production of giant gourami Room’ in this issue. their welfare. Physiology & Behavior 92. https://doi.org/10.1016/j.aquaculture. Fosseidengen J E, A Fernö, and van den • Due to the high number of farmed (Osphronemus goramy): Current rearing Stress and Welfare in Farm Animals: 375– 2009.09.030. [19] McCulloch S P, 2013. A Critique of Bos R, 2008. Learning in cod (Gadus fish species and the too big chal- practices and recommendations for fu- 397. https://doi.org/10.1016/j.phys- FAWC’s Five Freedoms as a Framework for morhua): long trace interval retention. lenge to research them all in de- ture research. Journal of the World Aqua- [12] Rahman M M, Islam Md S, Halder beh.2007.02.003. the Analysis of Animal Welfare. Journal of Animal Cognition 11: 215–222. https:// tail, we advocate focusing research culture Society n/a: 20. https://doi. G C, and Tanaka M, 2006. Cage culture Agricultural and Environmental Ethics 26: [29] Kittilsen S, 2013. Functional aspects doi.org/10.1007/s10071-007-0103-6 and farming on a small number of org/10.1111/jwas.12647 — see also of sutchi catfish, Pangasius sutchi (Fowler 959–975. https://doi.org/10.1007/ of emotions in fish.Behavioural Processes species. the FishEthoBase profile of Osphronemus 1937): effects of stocking density on [37] Studer B HP, 2015. How does Fish- s10806-012-9434-7. 100: 153–159. https://doi.org/10. goramy: http://fishethobase.net/ growth, survival, yield and farm profita- EthoBase define fish welfare?Database. 1016/j.beproc.2013.09.002. db/68/) bility. Aquaculture Research 37: 33–39. [20] Huntingford F A and Kadri S, 2014. FishEthoBase. https://doi.org/10.1111/j.1365- Defining, assessing and promoting the wel- [30] Fife-Cook I and Franks B, 2019. [6] Bosakowski T and Wagner E J, 1995. [38] Saraiva J L, Castanheira M F, 2109.2005.01390.x — see also the fare of farmed fish.Revue Scientifique et Posi-tive Welfare for Fishes: Ration- Experimental use of cobble substrates in Arechavala-Lopez P, Volstorf J, and FishEthoBase profile of Pangasianodon Technique de l’OIE 33: 233–244. https:// ale and Areas for Future Study. Fishes concrete raceways for improving fin condi- Studer B HP, 22018. Domestication and hypophthalmus: http://fishethobase.net/ doi.org/10.20506/rst.33.1.2286. 4: 31. https://doi.org/10.3390/ tion of cutthroat (Oncorhynchus clarki) and Welfare in Farmed Fish. In Animal Domesti- db/33/ fishes4020031 — see also the contri- rainbow trout (O. mykiss). Aquaculture 130: [21] Saraiva J L, Arechavala-Lopez P, cation, 109–135. London: IntechOpen. bution of Becca Franks er al. on ‘What 159–165. https://doi.org/10.1016/ [13] Szkudlarek M and Zak s´ Z, 2007. Castanheira M F, Volstorf J, and Studer about joy?’ in this issue. [39] see Billo Heinzpeter Studer’s contribu- 0044-8486(94)00223-B — see also the Effect of stocking density on survival and B H, 2019. A Global Assessment of Wel- tion on ‘Farmed fishes: Why so many?’ in FishEthoBase profile of Oncorhynchus my- growth performance of pikeperch, Sander fare in Farmed Fishes: The FishEthoBase. [31] Delcourt J, Becco C, Vandewalle N, this issue. kiss: http://fishethobase.net/db/30/) lucioperca (L.), larvae under controlled con- Fishes 4: 30. https://doi.org/10.3390/ and Poncin P, 2009. A video multitracking [7] Davis O A and Ansa E, 2010. Com- ditions. Aquaculture International 15: 67– fishes4020030 — see also http://fisheth- system for quantification of individual be- [40] Fatollahi M and Kasumyan A O, parative assessment of water quality 81. https://doi.org/10.1007/s10499- obase.net havior in a large fish shoal: Advantages 2006. The study of sensory bases of the 006-9069-7 — see also the FishEtho- and limits. Behavior Research Methods feeding behavior of the African catfish parameters of freshwater tidal earthen [22] Short profiles rationale: http:// Base profile of Sander lucioperca: http:// 41: 228–235. https://doi.org/10. Clarias gariepinus (Clariidae, Siluri- ponds and stagnant concrete tanks for fish fishethobase.net/media/statements/ra- fishethobase.net/db/42/ 3758/BRM.41.1.228 — see also the formes). Journal of Ichthyology 46: S161– production in Port Harcourt, Nigeria. Inter- tionale_short_profiles.pdf FishEthoBase profile of O. niloticus http:// S172. https://doi.org/10.1134/ national Journal of Science and Nature 1: [14] Datta S N, Dhawan A, Kumar S, [23] http://fishethobase.net/db/10/ fishethobase.net/db/31/ S0032945206110051. 34–37. Singh A, and Parida P, 2017. Standardi- findings/#ref_7 [8] Njoku O E, Agwa O K, and Ibiene zation of stocking density for maximizing [32] Kolarevic J, Aas-Hansen Ø, Esp- [41] Strand Å, Magnhagen C, and A A, 2015. An investigation of the micro- biomass production of Pangasius pangasius [24] http://fishethobase.net/db/10/rec- mark Å, Baeverfjord G, Terjesen B F, and Alanärä A, 2007. Effects of repeated dis- biological and physicochemical profile in pond cage aquaculture. Journal of Environ- ommendations/#ref_2 Damsgård B, 2016. The use of acoustic turbances on feed intake, growth rates and mental Biology 38: 37–242 — see acceleration transmitter tags for monitor- energy expenditures of juvenile perch, Per- of some fish pond water within the Niger [25] Rodríguez S R, Regalado E M, also the FishEthoBase profile of P. hypo- ing of Atlantic salmon swimming activity ca fluviatilis. Aquaculture 265: 163–168. Delta region of Nigeria. African Journal of Calderón Pérez J A, Núñez Pastén A, and phthalmus:http://fishethobase.net/ in recirculating aquaculture systems (RAS). https://doi.org/10.1016/j.aquaculture. Food Science 9: 155–162. Solís Ibarra R, 2007. Comparison of some db/33/ Aquacultural Engineering 72–73: 30–39. 2007.01.030. reproductive characteristics of farmed and

52 I FROM THE RESEARCH I 53 FROM THE RESEARCH

[42] Kittilsen S, Ellis T, Schjolden J, Braas- [50] Barreto R E, Arantes Carvalho G G, Noise and Musical Stimuli on Growth Per- Animal Behaviour Science 87: 343– [73] Batzina A and Karakatsouli N, tad B O, and Øverli Ø, 2009. Determin- and Volpato G L, 2011. The aggressive formance and Feed Utilization of Koi fish 354. https://doi.org/10.1016/j.ap- 2012. The presence of substrate as a ing stress-responsiveness in family groups behavior of Nile tilapia introduced into (Cyprinus carpio) in Recirculating Water planim.2004.01.004. means of environmental enrichment in of Atlantic salmon (Salmo salar) using novel environments with variation in enrich- Conditions. Turkish Journal of Fisheries and intensively reared gilthead seabream [65] Huntingford F A, Andrew G, non-invasive measures. Aquaculture 298: ment. Zoology 114: 53–57. https://doi. Aquatic Sciences 19: 513–523. Sparus aurata: Growth and behavioral Mackenzie S, Morera D, Coyle S M, 146–152. https://doi.org/10.1016/j. org/10.1016/j.zool.2010.09.001. effects. Aquaculture 370–371: 54–60. [58] Nawang S U S M, Ching F F, and Pilarczyk M, and Kadri S, 2010. Cop- aquaculture.2009.10.009. https://doi.org/10.1016/j.aquacul- [51] Castanheira M F, Herrera M, Cos- Senpo S, 2019. Comparison on growth ing strategies in a strongly schooling ture.2012.10.005. [43] Benhaïm D, Péan S, Brisset B, Leguay tas B, Conceição L E C, and Martins performance, body coloration changes fish, the common carp Cyprinus carpio. D, Bégout M L, and Chatain B, 2011. C I M, 2013. Linking cortisol responsive- and stress response of juvenile river catfish, Journal of Fish Biology 76: 1576–1591. [74] Mustapha M K, Oladokun O T, Sal- Effect of size grading on sea bass (Dicen- ness and aggressive behaviour in gilt- Pangasius hypophthalmus reared in differ- https://doi.org/10.1111/j.1095- man M M, Adeniyi A I, and Ojo D, 2014. trarchus labrax) juvenile self-feeding behav- head seabream Sparus aurata: Indication ent tank background colour. Aquaculture 8649.2010.02582.x. Does light duration (photoperiod) have an iour, social structure and culture performance. of divergent coping styles. Applied Ani- Research 50: 2591–2599. https://doi. effect on the mortality and welfare of cul- [66] Martins C I M, Castanheira M F, Aquatic Living Resources 24: 391–402. mal Behaviour Science 143: 75–81. org/10.1111/are.14215. tured Oreochromis niloticus and Clarias Engrola S, Costas B, and Conceição https://doi.org/10.1051/alr/ https://doi.org/10.1016/j.applanim. gariepinus? Turkish Journal of Zoology 38: [59] van de Nieuwegiessen P G, Boer- L E C, 2011. Individual differences in 2011140. 2012.11.008 – see Maria Filipa Castan- 466–470. lage A S, Verreth J A J, and Schrama J W, metabolism predict coping styles in fish. heira's contribution on ‘Coping styles, a [44] Barreto R E and Volpato G L, 2006. 2008. Assessing the effects of a chronic Applied Animal Behaviour Science 130: [75] Mercier L, Racotta I S, Yepiz‐ tool to better understand fish welfare’ in this Ventilatory frequency of Nile tilapia sub- stressor, stocking density, on welfare indi- 135–143. https://doi.org/10.1016/j. Plascencia G, Muhlia‐Almazán A, Civera issue. jected to different stressors. Journal of Ex- cators of juvenile African catfish, Clarias applanim.2010.12.007. R, Quiñones‐Arreola M F, Wille M, perimental Animal Science 43: 189–196. [52] Hecht T and Appelbaum S, 1988. gariepinus Burchell. Applied Animal Sorgeloos P, and Palacios E, 2009. [67] Shapovalov L and Taft A C, 1954. https://doi.org/10.1016/j.jeas. Observations on intraspecific aggression Behaviour Science 115: 233–243. Effect of diets containing different levels of The Life Histories of the Steelhead Rain- 2006.05.001. and coeval sibling cannibalism by larval https://doi.org/10.1016/j.ap- highly unsaturated fatty acids on physio- bow Trout (Salmo gairdneri gairdneri) and juvenile Claias gariepinus (Clarii- planim.2008.05.008. logical and immune responses in Pacific [45] Barreto R E and Volpato G L, 2004. and Silver Salmon (Oncorhynchus kisutch) dae: Pisces) under controlled conditions. whiteleg shrimp Litopenaeus vannamei Caution for using ventilatory frequency as [60] Rebensburg P, 2010. Assessment With Special Reference to Waddell Journal of Zoology 214: 21–44. https:// (Boone) exposed to handling stress. Aqua- an indicator of stress in fish. Behavioural and evaluation of temperament traits in Creek, California, and Recommendations doi.org/10.1111/j.1469-7998.1988. culture Research 40: 1849–1863. Processes 66: 43–51. https://doi.org/ carp (Cyprinus carpio L.), with contrasts Regarding Their Management. Fish Bulletin tb04984.x. https://doi.org/10.1111/j.1365- 10.1016/j.beproc.2004.01.001. between mirror and scaled morphological 98. STATE OF CALIFORNIA DEPARTMENT 2109.2009.02291.x. [53] Brown G E and Smith R J F, phenotypes. Diploma thesis, Berlin: Free OF FISH AND GAME. [46] Reilly S C, Quinn J P, Cossins A R, 1997. Conspecific skin extracts elicit anti- University of Berlin. [76] Buch Hang B T, Thanh Phuong N, and Sneddon L U, 2008. Behavioural [68] Yano I, Kanna R A, Oyama R N, predator responses in juvenile rainbow trout and Kestemont P, 2014. Can immunostimu- analysis of a nociceptive event in fish: [61] Mesquita F O, Borcaro F L, and Hunt- and Wyban J A,1988. Mating behav- (Oncorhynchus mykiss). Canadian Journal lants efficiently replace antibiotic in striped Comparisons between three species ingford F A, 2015. Cue-based and algo- iour in the penaeid shrimp Penaeus of Zoology 75: 1916–1922. https://doi. catfish (Pangasianodon hypophthalmus) demonstrate specific responses. Applied rithmic learning in common carp: A possi- vannamei. Marine Biology 97: 171–175. org/10.1139/z97-821. against bacterial infection by Edwardsiella Animal Behaviour Science 114: 248– ble link to stress coping style. Behaviour- https://doi.org/10.1007/ ictaluri? Fish & Shellfish Immunology 40: 259. https://doi.org/10.1016/j.ap- [54] Gregory T R and Wood C M, 1999. al Processes 115: 25–29. https://doi. BF00391299. 556–562. https://doi.org/10.1016/j. planim.2008.01.016. Interactions between individual feeding org/10.1016/j.beproc.2015.02.017. [69] Mendonça F Z, Volpato G L, Cos- fsi.2014.08.007. behaviour, growth, and swimming perfor- [47] Kaiser H, Weyl O, and Hecht T, [62] Jones C, Alberto H, Noble C, ta-Ferreira R S, and Gonçalves-de-Freitas mance in juvenile rainbow trout (Onco- [77] Hoseinifar S H, Soleymani N, and 1995. Observations on agonistic beha- Damsgård B, and Pearce G P, 2012. In- E, 2010. Substratum choice for nesting in rhynchus mykiss) fed different rations. Ringø E, 2014. Effects of dietary fruc- viour of Clarias gariepinus larvae and ju- vestigating the influence of predictable male Nile tilapia Oreochromis niloticus. Canadian Journal of Fisheries and Aquatic to-oligosaccharide supplementation veniles under different densities and and unpredictable feed delivery sched- Journal of Fish Biology 77: 1439–1445. Sciences 56: 479–486. https://doi. on the growth performance, haemato- feeding frequencies in a controlled en- ules upon the behaviour and welfare of https://doi.org/10.1111/j.1095- org/10.1139/f98-186. immunological parameters, gut microbio- vironment. Journal of Applied Ichthyo- Atlantic salmon parr (Salmo salar) using 8649.2010.02754.x. ta and stress resistance of common carp logy 11: 25–36. https://doi.org/ [55] Bégout Anras M L and Lagardère social network analysis and fin damage. [70] Baron V D, Orlov A A, and (Cyprinus carpio) fry. British Journal of Nu- 10.1111/j.1439-0426.1995.tb00003.x. J P, 2004. Measuring cultured fish swim- Applied Animal Behaviour Science 138: Golubtsov A S, 1994. African Clarias cat- trition 112: 1296–1302. https://doi. ming behaviour: first results on rain- 132–140. https://doi.org/10.1016/j. [48] Almazán-Rueda Pablo, Schrama fish elicits long-lasting weak electric pulses. org/10.1017/S0007114514002037. bow trout using acoustic telemetry in applanim.2012.01.019. J W, and Verreth J A J. 2004. Behavioural Experientia 50: 644–647. https://doi. tanks. Aquaculture 240: 175–186. responses under different feeding methods [63] Taylor J, Vinatea L, Ozorio R, org/10.1007/BF01952864. https://doi.org/10.1016/j.aquacul- and light regimes of the African catfish Schuweitzer R, and Andreatta E R, 2004. ture.2004.02.019. [71] Longrie N, Van Wassenbergh S, (Clarias gariepinus) juveniles. Aqua- Minimizing the effects of stress during Vandewalle P, and Mauguit Qand Par- culture 231: 347–359. https:// [56] Bui S, Oppedal F, Korsøen Ø J, eyestalk ablation of Litopenaeus vannamei mentier E, 2009. Potential mechanism doi.org/10.1016/j.aquacul- Sonny D, and Dempster T, 2013. Group females with topical anesthetic and a of sound production in Oreochromis nilo- ture.2003.11.016. Behavioural Responses of Atlantic Salmon coagulating agent. Aquaculture 233: ticus (Cichlidae). Journal of Experimental (Salmo salar L.) to Light, Infrasound and 173–179. https://doi.org/10.1016/j. [49] Valdimarsson S K and Metcalfe N B, Biology 212: 3395–3402. https://doi. Sound Stimuli. PLoS ONE 8: e63696. aquaculture.2003.09.034. 2001. Is the level of aggression and dis- org/10.1242/jeb.032946. https://doi.org/10.1371/journal. persion in territorial fish dependent on light [64] Yue S, Moccia R D, and Duncan pone.0063696. [72] Reyes-Tomassini J J, 2009. Behavio- intensity? Animal Behaviour 61: 1143– I J H, 2004. Investigating fear in domestic ral and Neuroendocrine Correlates of Sex 1149. https://doi.org/10.1006/anbe. [57] Kusku H, Ergun S, Yilmaz S., Guroy rainbow trout, Oncorhynchus mykiss, us- Change in the Gilthead Seabream (Sparus 2001.1710. B, and Yigit M, 2018. Impacts of Urban ing an avoidance learning task. Applied aurata). University of Maryland.

54 I FROM THE RESEARCH I 55 FROM THE RESEARCH FROM THE RESEARCH

2896 M. Mendl et al. Review. Animal emotion and mood adding phosphate to integrated aquaponic suggests a novel method to analyse pain punishment arousal or depression. The conscious subjective experience of systems as a fertilizer can have negative ef- responses to standard experimental proce- reward Welfare of fish — avoidance high emotions is what we are ultimately concerned about acquisition no longer the elephant in fects in African catfish (Clarias gariepinus), dures in this species. Using fractal analysis system when we consider human and animal welfare, and it is fearful system the room 1 not only on their welfare but also on the of behaviour, the authors create (and val- excited these subjective experiences that define the field of meat quality. These two studies emphasize idate) a pain intensity scale for zebrafish, anxiousous emotion research. In humans, the ‘gold standard’, albeit indirect, method for measuring these experiences is lin- a correlation that should be clear for the and propose that variations in complexity happy João L. Saraiva (PhD), Q1 guistic self-report. Statistical analyses of these reports fish industry: when the welfare of animals of movement should be a good indicator Q4 suggest that emotions can be defined in terms of two Pablo Arechavala-Lopez (PhD) fundamental underlying dimensions (e.g. Stanley & is improved, both the quality of the product of welfare in this species [6]. This paper –ve +ve valence Meyer 2009). Emotional experiences are valenced—they Fish Ethology and Welfare Group, and its value increase – a rare case when also adds compelling evidence that fish are are perceived as positive or negative, rewarding or Centro de Ciencias do Mar (CCMAR), the interest of the industry and the ethical sentient and able to feel pain. Both studies sad punishing, pleasant or unpleasant—neutral states are Q2 not emotional states. Emotional experiences also vary in Rua José Mateus Horta 3, standards underlying its activity walk hand dive into the biology of welfare in zebraf- Q3 relaxed depressed reported activation or arousal. For example, the states 38000-536 Faro, Portugal in hand. ish, using basic behavioural variables and calm of elation and contentment are both positively valenced, [email protected] knowledge on the ethology of the species This study highlights the need to take into but the former involves a higher degree of arousal than [email protected] to highlight the importance of the natural low the latter. account the age of the individuals when [5] and mental [6] dimensions of welfare. Subjective experiences that can be characterized in The concept of fish welfare is fairly recent designing prevention and treatment plans Figure 1. Core affect represented in two-dimensional space. terms of these valence and arousal dimensions have Figure 1:Words Core ineffect italics depicted indicate in two-dimensional possible locations space. of specific Italic Figure 2: Hypothetical examples of how an organism's core affective and was overlooked for many years, based as well as rearing routines. The study by The importance of understanding the ethol- been labelled core affect (Russell 2003; Barrett et al. terms indicatereported possible affective locations states (including of specific discrete/basic reported emotions). affective states2007 ).state They can can change be represented over time. inThe two-dimensional right green loop represents changes Positive affective states are in quadrants Q1 and Q2, and on a popular misconception that fish were Moreira et al. [4] takes an ontogenic ap- ogy of reared species is further explored in space as shown in figure 1. Positive affective states lie in (includingnegative discrete/basic states in quadrantsemotions). Q3Positive and Q4.affective Arrows states indicate are located during successful cycles of reward acquisition. The left green loop ‘stupid’ creatures devoid of any kind of proach into amyloodiniosis, a well-known the review by Gonçalves-de-Freitas et al. in quadrantsputative Q1 biobehaviouraland Q2, and systemsnegative associated states in quadrants with reward Q3 andthe rightrepresents half of this changes space during (quadrants unsuccessful Q1 and cycles. Q2), and The red line represents sentience or mental capability. However, a health problem in white seabream (Diplo- [7], where the social behaviour of Nile ti- Q4. Arrowsacquisition indicate and putative the Q3–Q1 bioethological axis of core behavioural affect (green), systems and negativechanges affective that states occur in in the response left half to(Q3 the presence and Q4). (quadrant Q4) or Core affect can thus be conceptualized as the funda- growing body of research on fish research dus sargus) farmed in Southern Europe. lapia (Oreochromis niloticus) is proposed associatedpunishment with the avoidanceacquisition and of therewards Q2–Q4 (Q3 axis – Q1 of coreaxis affectof the core successful avoidance (Q2) of threats or punishment. (red). Adapted from Russell (e.g. Russell & Barrett 1999) mental subjectively reportable manifestation of any emotion made clear that this is evidently not the Focusing on fish health is not new in welfare as a key component in the welfare of this affect, green)and Panksepp or with (e.g.the avoidanceBurgdorf & of Panksepp punishment 2006 ).(Q2 – Q4 axis ofor moodFrom state, Mendl and et core al. [11]. affect space provides us with case—fish are sentient, socially complex research. After all, health is one of the key fish. In this study, the authors thoroughly re- the core affect, red). From Mendl et al. [11]. a way of conceptualizing the structure of subjective animals that have highly developed mental components for the conceptual framework view the social ethology of tilapia, elegant- emotional experiences. Discrete emotions such as fear, sadness and happiness are located somewhere in this Izard 2007; Panksepp 2007). It is not our aim to argue in abilities as well as the neural substrate to of welfare, together with the mental and nat- ly addressing both proximate and ultimate space, although their location per se does not fully encap- the positivesupport class of one of orexperiences other. Rather, are we cur believe- Can that theyfishes can experience and salience (i. e. appetitive predictable, support them. As this evidence grew larger, ural components. The novelty of this paper mechanisms to provide operational insights sulate their subjective qualities. For example, a highly be brought together to provide a conceptual framework 2 rently being neglected in fish and urge for happiness? aroused negatively valenced stateappetitive (Q4) accompanied unpredictable, by aversive pre- the uncomfortable questions regarding the is to search for a non-veterinary approach that may improve its welfare. The social en- for studying animal emotions that: (i) offers a structure more research in this area. an urge to flee may characterizedictable, fear while aversive a state of theunpredictable).’ In oth- for integrating disparate discrete emotions,It is providing true that ahappiness is a subjective eval- welfare state of fish and the ethical implica- to deal with a health issue, using one of vironment is demonstrated to have impacts same valence and arousal accompanied by an urge to functional perspective on the adaptive value of different er words, Sea bream displays all the major tions of fish farming became anelephant Tinbergen’s Four Questions (see box) that on stress levels, growth and aggression, Finally, Saraiva et al. [9] propose a frame- uation of an internalattack state, may so characterize the word anger.may emotional states, (ii) suggests how ‘free-floating’ mood emotional states, – including happiness. be misleading whenThe referring core affect to conceptanimals. is rooted in an understand- in the room that was difficult to ignore. is so often overlooked: development. The and the authors offer solutions to mitigate work tostates assess arise the welfare from short-term of farmed emotional fishes responses to ing of the subjective experience of emotion. While this However, there are recent indications that results show that young fish are far more the effects of rearing conditions: lighting, at a speciesevents, level: and howthe theyFishEthoBase may function. This to guideIt is also decision- true that positive emotional states 2 – Kittilsen [13] suggests positive emotions may lie at the heart of our interests in animal emotion, making, and (iii) yields novel hypothesis-drivenhave measures been receiving far less attention than things are changing, and the collection of susceptible to infection by Amyloodinium environment colour and enrichment struc- open-access database on fish ethology it raises challenges given that indirect fish measurementon page 157, of referring to studies in of animal emotion. negative, perhapssubjective for obvious states in reasons another human, let alone another papers in the recent book ‘Welfare of cul- ocellatum because they lack immune and tures are pinpointed as simple ways to and welfareIn developing aims to thisprovide framework, a tool we aimto to bring together cod: ‘The memory of this (positive) associa- species, is not currently possible. However, the reported tured and experimental fishes’ [1] suggests physiological responses that only appear reduce the detrimental effects of human-in- evaluateand the build welfare upon thestate ideas of of(ultimate many- other[10] researchers. That is why there is an objective defi- tion between light and the delivery of food subjective experiences of core affect in humans are of human and animal emotions (e.g. Langnitionet al .of 1990 emotional; states in animals [11] that all the interested parties (scientists, later in ontogeny. This study highlights the duced social disturbance. ly) all farmed species worldwide. In that accompanied by neural, behavioural,was retained physiological for andat least three months. Cabanac 1992; Gray 1994; Panksepp 1998; Cacioppo farmers, retailers, NGOs and consumers) need to take into account the age of the sense, the authors have built the portal which can be measuredcognitive changes,according such to asob alterations- It has inalso brain recently activity, been shown in cod The review by Fife-Cook and Franks [8] et al. 1999; Russell & Barrett 1999; Watson et al. 1999; jective indicators,facial as shown expressions, in figure heart .1 rate and attention to threat. are now directly approaching the subject. individuals when designing prevention and www.fishethobase.netNesse 2000, 2004 where, 2005 an; Carver impressi 2001- ; Ellsworth & that environmental enrichment promotes a proposes a framework for positive welfare These changes can be measured objectively. Together Ladies and gentlemen, the elephant has left treatment plans as well as rearing routines. ve amountScherer of data 2003 ;concerningRolls 2005; theNesse biology & Ellsworth 2009). We higher propensity for exploration of novel From this figurewith and subjective definition, experience, we can they make up the components in fish (i. e., mental and physical states that start by outlining the dimensional approach, which has the building. of farmed species and the impacts of aqua- of emotional or affective states.areas Researchers and socially can study facilitated learning’. Zebrafish welfare was another surprisingly exceed what is necessary for immediate received limited attention in animal emotionpredict research that an animal is ‘happy’ if he is these measurable components of animal emotions, culture on(but their see welfareGray 1994is scrutinised,), then briefly orga- summarizeexperiencing some high arousal and a positive In fact, the papers in [1] are a fantastic ignored issue until recent times. The number survival), which would replace the tradi- and attempt to identify those3 components– Braithwaite that et al are [14] dive deeply into nised anddisagreements summarised. between Using discrete the data and dimensionalon theorists internal state (the reliablyQ1 in the associated figure 2) with. Since particular locations in core example of the many perspectives that may of cultured individuals arguably surpasses tional paradigms that focus on mitigating before suggesting how the two approaches may be the evidence for cognition and emotional sta- 41 species already available, the authors affect space. be used when tackling fish welfare. In a any other commercially farmed species, the negative impacts of rearing. The pos- brought together. We end by consideringwe implications cannot ask the animal directly (in this tes in fish, describing why there are differen- analyse their welfare state and conclude Of course, even if we can use measurable components for the assessment of animal emotion,case including the fish), the this can be assessed through pilot study regarding fisheries of catshark yet even when the subject of welfare in itive welfare approach requires a deep of emotional responses to locateces an among animal’s species position but in highlighting in page that (i) thedevelopment general welfare of new measuresstate of farmed that may be particularly (Scyliorhinus canicular), Barragán-Méndez aquaculture started to be addressed, ze- understanding of the species’ behaviour indicators: brain coreactivity affect in space,the reward we cannot sys- be16: certain ‘The that example they experi- of pain and suffering fishes isuseful poor, for (ii) assessing there long-termis some moodpotential states. et al. [2] demonstrate that the standard brafish were apparently left behind. Now, and biology and would demand taxa-spe- tem, behaviours, encehormones, the conscious etc. component too.above Whether indicate or not, emotions and in a negative do- for improvement, and (iii) this potential practices of exposing the wild-caught an- two studies by Woodward et al. [5] and cific standards. However, the knowledge to what extent, different speciesmain, experience but little conscious is known about the potential is related to research on species’ needs, From this groundwork,affective all states the remainspapers anthat area I of intense and unresolved imals to air are not only extremely harmful Deakin et al. [6] focus on two important already available from fish and other taxa for positive, or pleasurable, effects in fish. but (iv) 2.there A DIMENSIONAL are many remaining VIEW OF THEknow STRUCTURE- suggested presentdebate compelling (e.g. Wemelsfelder evidence 1997 ; Macphail 1998; Baars for the fish but also modify muscle texture topics that impact zebrafish welfare: the allows both the identification of positive OF EMOTION: CORE AFFECT 2001; Rolls 2005). For the purposesHowever, and scopegiven of that this fish possess similar ledge gaps, and (v) current fish farming that fish can experience postitive emotion- properties and reduce the quality of the first shows that environmental enrichment welfare states in fish and the suggestion of (a) Core affect and subjective emotional experience paper, however, we must leave thisgeneral to one side,neural discussing systems that modulate the technologiesEmotions do not interest seem us to because fully address of their distinctiveal states: con- animal emotions as states that may or may not be meat. This study demonstrates the urgency in zebrafish housing promotes aggression active measures: species-specific housing feeling of well-being and seeking positive welfarescious issues. manifestation—the feelings of joy, relief, anxiety experienced consciously. of improving the welfare of wild-caught and risk-taking behaviours in zebrafish (including ambient colour and appropriate 1 – Cerqueira et al [12] state in page 6: reinforcement that are found in mamma- fish and indicates the road ahead regard- [5], and the authors explain this with the social environment, as already suggested Fish welfareProc. R. seems Soc. B (2010)to have gained a con- ‘In this study we have shown that Sea lian brains (e. g., the serotonergic and ing the assessment of humane practices in social and territorial behaviour of the spe- in [7]) and the promotion of cognitive siderable momentum and, although there bream exposed to stimuli that vary ac- dopaminergic systems), the capacity for fisheries. The paper byStrauch et al. [3] cies, in which the enrichment structures pro- engagement (visual stimulation, novel ob- is yet much work ahead, we can optimisti- cording to valence (appetitive, aversive) positive feelings in fish would seem likely.’ also highlights how a common practice of vide resources to monopolise; the second jects, play, etc.). The authors conclude that cally say that the wind is blowing in a and salience (predictable, unpredictable) 4 – Franks et al [15] actually present be- favourable direction. exhibit different behavioural, physiolog- ical and neuromolecular states that are havioural evidence for positive emotions 1 The article originally appeared as an introduction to the special issue ‘Welfare of Cultured and Experimental Fishes’ of specific to each combination of valence in zebrafish. In the summary on page 1, the journal Fishes [1]. Courtesy of the publisher and authors. 2 Explanation by João L. Saraiva (2019) to a sceptical fish farmer

56 I FROM THE RESEARCH I 57 FROM THE RESEARCH

the authors suggest: ‘Collectively, these References [11] Mendl M, et al, 2010. An integrative Box Take Home Message results are similar to the patterns that [1] Arechavala-López P A, Saraiva J L, and functional framework for the study of typify positive emotional behavior in oth- 2019. Welfare Of Cultured And Experi- animal emotion and mood, Proc. R. Soc. B Tinbergen’s Four Questions For a long time fish were seen as ‘stu- er animals, for example, social groom- mental Fishes. Basel, Switzerland: MDPI; (2010) 277, 2895–2904 ing and social play’ and on page 10, of Ethology, applied to fish pid’ creatures without any kind of sen- (2019), ISBN 978-3-03921-711-3 (PDF) [12] Cerqueira M, Millot S, Castanheira they conclude: ‘Our results suggest that welfare [17] sibility. As the evidence for the mental M F, and Oliveira R F, 2017. Cognitive heightened-shoaling episodes may be In 1963, Nikolaas Tinbergen pub- abilities of fish grew, the uncomforta- [2] Barragán-Méndez C, Sánchez- appraisal of environmental stimuli induces another promising area of inquiry for fu- lished a groundbreaking model for ble questions about fish welfare and García F, Sobrino I, Mancera JM, and emotionlike states in fish. Scientific reports, ture investigations into positive emotions in the study of animal behaviour: the its ethical implications for fish farming Ruiz-Jarabo I, 2018. Air Exposure in 7(1), 13181, page 6. https://www.na- zebrafish.’ Four Questions of Ethology [18]. This became an ‘elephant in the room’ that Catshark (Scyliorhinus canicula) Modify ture.com/articles/s41598-017-13173-x central idea sets out the four levels of no one wanted to address. Recently, Muscle Texture Properties: A Pilot Study. 5 – Brown [16] reviews and discusses (open access) analysis that provide an integrative ap- however, there have been increasing Fishes, 3, 34., in [1] cognitive abilities in fish. While not directly proach to any behavioural question. signs that all interested parties — sci- [13] Kittilsen S, 2013. Functional aspects referring to positive emotional states, there [3] Strauch S M, Bahr J, Baßmann B, In aquaculture, these questions can be entists, fish farmers, retailers, NGOs Bischoff A A, Oster M, Wasenitz B, of emotions in fish. Behavioural processes, are many references to emotions in fish in a and consumers — now want to ad- applied to seek and offer solutions for and Palm H W, 2019. Effects of Ortho- 100, 153–159, insbes. S. 157. https:// comparative and functional approach. dress the issue directly. fish welfare based on sound science. Phosphate on Growth Performance, www.researchgate.net/profile/Silje_Kit- 6 – Finally, Fife-Cook and Franks [8] ex- tilsen/publication/256928588_Func- 1. Mechanism (causation): What stim- As the latest research shows, the issue Welfare and Product Quality of Juvenile tensively describe positive emotions in fish tional_Aspects_Of_Emotions_In_Fish/ uli elicit the behavioural responses to of fish welfare has gained considera- African Catfish (Clarias gariepinus). Fishes, and from page 6 onwards there is a whole links/5ba8e05692851ca9ed223ad9/ the farming conditions? What are the ble momentum. Studies show that the 4, 3., in [1] section dedicated to the topic. Page 7: Functional-Aspects-Of-Emotions-In-Fish.pdf molecular, neural, endocrine and over- quality and value of the product in- ‘Physiological evidence suggests that fish [4] Moreira M, Cordeiro-Silva A, Barata all physiological mechanisms behind crease when fish welfare is improved — [14] Braithwaite V A, Huntingford F, and possess the necessary anatomical and M, Pousão-Ferreira P, and Soares F, 2019. these behavioural responses? a rare case where industry inter- van den Bos R, 2013. Variation in emotion chemical structures to experience emo- Influence of Age on Stress Responses of est and ethical standards go hand and cognition among fishes. Journal of ag- tion’; page 8: ‘A number of behaviors, 2. Development (ontogeny): How does White Seabream to Amyloodiniosis. Fish- in hand. Other work is concerned ricultural and environmental ethics, 26(1), many of which have been documented the behaviour of farmed fishes change es, 4, 26., in [1] with ways of structurally enriching 7–23, insbes. S. 16. https://link.springer. in fish, can signal positive emotional ex- with age, and what early experiences the usually monotonous aquaculture [5] Woodward M A, Winder L A, and com/article/10.1007/s10806-011- perience in animals, including successful are necessary for these behaviours to habitat, creating opportunities for re- Watt P J, 2019. Enrichment Increases Ag- 9355-x (open access), coping, accessing reward, and success- develop? What are the relative roles treat but also challenges. Other stud- gression in Zebrafish.Fishes, 4, 22, in [1] [15] Franks B, Graham C, and von Keyser- ful goal-directed behavior.’; ‘grooming of genes versus the environment? Do ies shift the emphasis from avoiding [6] Deakin AG, Spencer JW, Cossins A R, lingk M, 2018. Is Heightened-Shoaling a represents another group activity that has these behaviours occur as in nature? negative experiences for the fish to been linked to positive emotion, such as Young I S, and Sneddon L U, 2019. Wel- Good Candidate for Positive Emotional Be- 3. Function (adaptation): How does promoting positive fish welfare, i. e. inducing a relaxed state in fish and oth- fare Challenges Influence the Complexity havior in Zebrafish?. Animals, 8(9), 152. the behaviour influence the animal’s fit- mental and physical conditions that er vertebrates. In fish, it has been shown of Movement: Fractal Analysis of Beha- https://www.mdpi.com/2076-2615/ ness in the wild? How does it influence go beyond what is necessary for im- that tactile stimulation can lower stress viour in Zebrafish. Fishes, 4, 8., in [1] 8/9/152 (open access) the animal's welfare under farming con- mediate survival — an approach that levels and facilitate future pro-social in- ditions? Is the behaviour performed in calls for more research, since positive [7] Gonçalves-de-Freitas E, Bolognesi M [16] Brown C, 2015. Fish intelligence, teractions. Taken as a whole, these lines the same context as in the wild? emotional states have so far received C, dos Santos Gauy A C, Brandão M L, sentience and ethics. Animal cognition, of research indicate that, under certain far less attention than negative ones. Giaquinto P C, and Fernandes-Castilho 18(1), 1–17. https://link.springer.com/ circumstances, the presence of a conspe- 4. Evolution (phylogeny): How can the Finally, to avoid the danger of mis- M, 2019. Social Behavior and Welfare in article/10.1007/S10071-014-0761-0 cific and pro-social behavior is likely to behaviour be compared with that of leading interpretations from the sub- Nile Tilapia. Fishes, 4, 23., in [1] (open access) related species? What are the selection involve positive emotional responses in jective evaluation of ‘happiness’, one processes leading to this behaviour? [8] Fife-Cook I, and Franks B, 2019. Posi- [17] Sarava J L, 2017. Driving Mr Tinber- some species of fish.’ study proposes an objective definition How can farming conditions match tive Welfare for Fishes: Rationale and Areas gen: The four questions of ethology applied of emotional states in animals. these processes? for Future Study. Fishes, 4, 31., in [1] to fish welfare.Vortrag an der Summer Shoal Even though there is still a lot of work [9] Saraiva J L, Arechavala-Lopez P, 2017, http://fishethobase.net/summer- ahead, we can optimistically say that Castanheira M F, Volstorf J, and Studer B H, shoal/2017/ the wind is blowing in a favourable 2019. A Global Assessment of Wel- fare [18] Tinbergen N, 1963. On Aims and direction. in Farmed Fishes: The FishEthoBase. Fishes, Methods of Ethology. Zeitschrift für Tier- 4, 30. [CrossRef] – see also the contribu- psychologie, 20: 410–433. tion of Jenny Volstorf et al. on ‘Knowledge as prerequisite for fish welfare’ in this issue [10] Franks B, et al, 2018. Fish are smart and feel pain: What about joy?, commen- tary on Sneddon et al. on Sentience Denial, Animal Sentience 2018.156 – see also the contribution of Becca Franks et al. on ‘What about joy?’ this issue

58 I FROM THE RESEARCH I 59 FROM THE FIELD

in direct interaction with practice. In this 1.1 Results of the first visits For criteria of low severity, we gave 9 recom- • No recommendations issued As expected, the easiest measures to im- Development of fish way we wanted to ensure that future fish to FOS aquaculture farms mendations to the companies, mainly con- after first visit, therefore no second visit plement are those to reduce stress. At the welfare guidelines for welfare guidelines were: Between January 2018 and March 2019 cerning hygiene and control: registration needed (2); second visit, 67 % of the companies to of visits (12 %), footbath and wheelbath whom we recommended they tackle this is- the ‘Friend of the Sea’ • feasible, we visited 51 fish farms belonging to • Second visit impossible, because the at the entrance (9 %), as well as measures sue were found to reduce or plan to reduce 33 companies in 12 countries (28 com- company had been severely damaged (FOS) certification * • controllable, and to improve data collection. stress by handling procedures, to limit the panies in 8 EU member states, 3 com- by storms (1); panies in Turkey, 1 company in Panama, time the fish spend out of water to a maxi- Billo Heinzpeter Studer 1, 2, • relevant for specific fish. 1 company in Chile). The reports con- 1.2 First consequences: Humane • The management changed after the mum of 15 seconds, to reduce the number Maria-Filipa Castanheira 3 (PhD), This plan convinced the Silicon Valley- tained an average 4.5 recommendations slaughter and fish welfare first visit and showed no interest (1); of sorting processes during the fish’s life Pablo Arechavala-López 2 (PhD), Open Philanthropy Pro- based foundation per farm. training cycle or to harvest the fish using pumps João Luis Saraiva 2 (PhD), • No reply or refusal of the demand for ject (OP) [2], which aims to promote ani- We were astonished by the high percent- instead of nets. 50 % of these companies Jenny Volstorf 2 (PhD) In criteria with high severity, the most fre- a second visit for unknown reasons (4). mal welfare in aquaculture. In this context, age of three quarters of the companies already have a solution at work. quent recommendation was for stunning 1  fair-fish international (Chair), OP awarded project contribu-tions to vari- visited, which harvest the fish without The results of the second visits represent the before slaughter (in 73 % of all compa- 47 % of the companies to whom we recom- Via delle Giarrette 109, ous certification programs(including ASC anaesthetising them afterwards. On the vast majority of cases. nies), followed by stress reduction during mended pre-slaughter stunning were found 34074 Monfalcone, Italy or GAA/BAP) and NGOs (including the one hand, these are mainly breeding Sea handling and harvesting (48 %), envi- During the visit or interview, we checked at the second visit to be seriously planning [email protected] Albert Schweitzer Foundation) before the bream (Sparus aurata) and Sea bass ronmental enrichment (36 %), reduction which of the recommended improvements to implement a stunning procedure; 11 % end of 2017, thus launching a unique com- (Dicentrarchus labrax) in the Mediterrane- 2 Fish Ethology and Welfare Group, of density (15 %) or of crowding (12 %), had been implemented or were at least of these companies meanwhile had aready petitive boost for fish welfare standards. an, for which we propose solutions with CCMAR, University of Algarve, improving light conditions (12 %), and under serious consideration, and which implemented electric stunning. Twenty years after the first efforts of fair-fish electric anaesthesia, which have now Campus de Gambelas, water quality control (12 %). A further were not, and for what reasons. To get an in Switzerland and Vissenbescherming in been implemented or are under serious 43 % of the companies to whom we recom- 8005-139 Faro, Portugal 18 recommendations, each with less than overview of the situation, we scored the re- Holland, the long neglected and smiled at examination (see section 2.3). On the mended to get fish welfare training report- [email protected] 10 % of the companies, require in particu- actions of the companies as follows: topic finally received broad support. other hand, many smaller trout farms in ed at the second visit currently examining 3 lar the dimensions of the housing system to • Improvement implemented: Score = 1.0 participation, in many cases by participa- Independent Welfare Consultant Work started in early 2018 with the first Northern Italy are sceptical about electric the needs of the species, and daily removal tion in our Fish Welfare Course; 14 % of (former member of the Fish Ethology site visits and continued until late summer stunning because they fear a loss of qual- • Improvement under serious and killing of moribund fish. these companies have already found a and Welfare Group), 2020 with the handover of the criteria ity (haemorrhaging) and higher operating consideration: Score = 0.5 solution (one company has solved the prob- Carrer de Benet Cortada 58,1,1, and indicators for the last of 24 species. For criteria of medium severity, the lack costs. However, these companies are • Measures neither implemented lem by having three of its employees com- 08174 Cugat del Valles, Spain In early 2019, the work was officially of training of personnel in fish welfare aware that slaughtering trout without an- nor considered: Score = 0.0 plete a specialist training course, whereas [email protected] taken over by our newly founded spin- issues (in 82 % of all companies) came aesthesia could lead to market losses in the first by far, followed by alack of observa- future. Colleagues from a Northern Italian the quality manager has also completed a In May 2017, fair-fish international, own- off Fish Ethology and Welfare Group At the second visit after about six months, tion and noting of fish welfare indicators research institute have therefore developed fish veterinary course). er of the FishEthoBase [1], together with (FishEthoGroup) [3], based at the CCMAR the 25 companies had already implement- (15 %) and a lack of traceability of stress- an alternative to stunning by thermal shock, Friend of the Sea (FOS), one of the leading Marine Research Institute of the University ed 17 % of all the recommendations we As expected, more difficult to tackle are ful measures like handling of fish, etc. which is being tested experimentally by our labels for sustainable fishing and aquacul- of the Algarve in Faro, under an agree- had made to them, and 37 % companies those recommendations that intervene more (12 %). The remaining 3 recommendations FishEthoGroup in comparison to stunning ture, agreed on a cooperation with the fol- ment between CCMAR and fair-fish were in the planning stage. While these strongly in the operational process, such as in this category concerned only 3 % of all with electricity, with MS222 and without lowing goal: international. companies had received an average of the installation of structures (substrate, hid- companies and also mainly concerned fish stunning. 4.6 recommendations per company, they ing places), the avoidance of crowding • to develop a set of core fish welfare cri- monitoring issues. reached an average improvement score of The lack of training of personnel in fish or the introduction of monitoring measures teria for all fish species kept on FOS- 2.5 per company. This means that these welfare issues observed in more than four- regarding behaviour, water quality and certified farms, with the aim of integrat- companies have implement-ed more than fifths of the companies has also led us to handling processes; see Fig. 4 for details. ing corresponding guidelines into the half of the improvements in six months or develop a Fish Welfare Course. The three- FOS certification standard, are currently seriously considering solu- day course for practitioners, auditors and 2. Development of fish welfare tions. If we relate this to the usual transition • developed on the basis of two visits to other interested parties from the industry criteria for the FOS-Standard periods for newly introduced label criteria FOS-certified companies. The first visit has been held for the first time in Novem- From the outset, Friend of the Sea had of one, two or even more years, the adjust- served a gap analysis between the sci- ber 2019 by experts at the headquarters decided to integrate the future fish welfare ment performance of these companies so entific knowledge gained and the ob- of FishEthoGroup at the Marine Research criteria as a binding component of its own far signals that an integration of fish welfare servations before species and ended in Institute CCMAR of the Universidade do standard and – in contrast to what the criteria criteria into the FOS certification a report to the farmer with recommen- Algarve in Portugal, with about 50 partici- Aquaculture Stewardship Council (ASC) standard is not unrealistic. This presuppos- dations on how he could improve the pants [4]. A second course will be held [5] appears to be doing – not to pur- es, of course, that the measures only under welfare of his fish. Half a year later, a online in spring 2021. sue an add-on strategy that would allow second visit was carried out to deter- planning so far will be implemented later individual farms to choose whether to mine which improvements had already 1.3 Improvements noted as well, let alone measures not yet taken subject themselves to animal welfare re- been successfully implemented or were during the second visits into account for the time being. quirements in addition to environmental in the planning stage and which had We were able to visit 25 of the 33 com- However, the fact that the FOS-certified com- ones. Friend of the Sea found it difficult to not, and for what reasons not. panies a second time or to interview them panies still face a challenging task communicate on the market one FOS label with and one without fish welfare add-ons. The decisive factor in our approach was by questionnaire or telephone (mainly com- becomes clear when we consider all 33 com- Figure 1: Recommendations to FOS fish farmers, by frequency Thus, the definition of fish welfare criteria not to develop guidelines at the table, but panies that had not yet addressed any of panies that were once visited: Of the total the recommendations). For 8 companies, a 145 recommendations made (an average applicable to all FOS farms faces the fact second visit or interview was not possible of 4.4 per company), only 20 (14 %) were that for some of the problems observed * Updated and translated version of a presentation on 28 Nov 2019 at the Annual Conference on Applied Ethology in Freiburg, for the following reasons: fully implemented during the second visits. there are no practical examples yet that Germany. A former version of the present report was published on 28 Jan 2020. a comparable farm could simply adopt.

60 I FROM THE FIELD I 61 FROM THE FIELD

Table 1: Example (extraxt) of a fish welfare criteria and criteria sheet for Friend of the Sea

European seabass — Ongrowing

13. Welfare requirements

13.01. Captive environment

No Requirement Level Indicators *

Production units should provide horizontal and There must always be 13.01.1 vertical withdrawel space, optimising fish welfare Essential horizontal and vertical conditions regarding spatial constraints. empty space.

Production units must not have sharp protrusions which may Absence of dangerous 13.01.2 Essential be injurious to the fish. protrusions.

Good overall condition Production units and equipment must be checked for holes, of nets and infrastructures. 13.01.3 faults and fouling. All equipment must be maintained regu- Essential Records of periodicity larly and recors must be ready for inspection. and methods.

Farm design should be such that inspection Water visibilty, ROVs, 13.01.4 Essential of all stock is possible. divers, cameras …

Optimal photoperiod for fish welfare must be determined on a site-by-site basis matching natural limits Facility allocated within and using practical experience, research the natural photoperiod 13.01.5 Essential and welfare specialist advice. and geographical range North Atlantic latitudes photoperiod max. range: of the species. 16L:8D-8L:16D

13.01.6 Important Depth net-pen.

Additional lighting either fixed or portable must Stock inspection 13.01.7 be available, but only should be switched to allow Important at all times. Figure 2: Implementation of our recommendations after half a year examination of the animals and equipment. Structural enrichment should be provided. If deemed Presence of enrichment — 13.01.8 impossible or harmful, other type of enrichment should be Recommended We therefore recommended that Friend of improve fish welfare step by step accord- in this category should be declared but observing 13.1.3 implemented (occupational, dietary, social, sensorial). the Sea (FOS) should not make such crite- ing to wise developments in practice, FOS mandatory in the future. ria mandatory until a farm with the same will classify the criteria into one of the fol- The cages should be located in a site protected This is the path on which currently recom- Absence of noise, recorded lowing three categories according to their from human induced noise. The maximum sound species and similar system has implement- with a hydrophone and mended criteria can be given a more 13.01.8 pressure level should be under 150 dB re 1µPa rms Important ed a recognised solution. This would be current feasibility: analysed with binding character in a next revision of the in the 0,2-1kHz frequency range in any point in line with the current situation of the long appropiate software. • ESSENTIAL: In the event of non-confor- standard. of the tank at all times. neglected fish welfare in aquaculture, mity identified by the auditor, the farm which has grown and still grows extremely For each of the 24 fish species (see table 5) will be given three months to rectify * Management-based indicators, see: Operational Welfare Indicators (OWI table) rapidly in terms of volume since the 1950s integrated into the project, the Fish- the problem. If the nonconformity per- and by farming a number of species EthoGroup developed a set of over 80 sists during a follow-up inspection, the eighteen times greater than in terrestrial criteria and indicators, each subdivided 3. Future research and consulting the FishEthoGroup has started to make its company loses the certificate. farming. into up to 5 production or life stages: eggs, activities services available to other players in the • IMPORTANT: In the case of a non-con- larvae, juveniles, adults, parent animals. aquaculture sector, like the ASC and the The aim is to improve the welfare of fish on At a meeting of the fish welfare projects formity identified by the auditor, the (See table 1 for an example). Spanish fish farming company Culmarex, as many FOS certified farms as possible supported by Open Philanthropy in April company will be given three weeks to in order to promote fish welfare. or to lose as few farms as possible when At deadline of this report (end of August 2019 in Brussels, it became clear that fair- present a corrective plan which must integrating welfare into the FOS standard. 2020) the experts of Friend of the Sea are fish international resp. its FishEthoGroup be carried out at the next inspection However, the FOS certification scheme in the process of integrating the recommen- had made the most progress in the devel- about one year later, otherwise the does not allow for the flexibility we pro- dations of the FishEthoGroup into a pro- opment of guidelines. At the beginning of company loses its certificate. posed. Similar to ASC, for example, any posal for the extension of the standard and 2020, Open Philanthropy complied with change or addition to the standard requires • RECOMMENDED: In the case of a non- preparing stakeholder consultation. our application for continued funding. a predetermined decision-making process conformity identified by the auditor, This allows the FishEthoGroup to support in which the representatives of the various the farm is free to follow a recommen- the implementation of the fish welfare cri- interest groups must agree, which is only dation for improvement. The auditor’s teria on the currently c. 100 FOS-certified possible on the basis of conclusively formu- reports on the behaviour of the farms aquaculture farms with research, con- lated proposals. Nevertheless, in order to are an indicator of whether a criterion sulting and training. At the same time,

62 I FROM THE FIELD I 63 FROM THE FIELD FROM THE FIELD

Links on achieving responsible and sustainable [7]. In a survey on options for a seven- Take Home Message [1] http://www.fishethobase.net/db Fish welfare indicators production by addressing an increasing teenth SDG, animal protection achieved for the ‘Aquaculture amount of issues that are impacted by aq- the second highest score [8] and the 2019 [2] https://www.openphilanthropy.org To date, there are no certifiable Stewardship Council’ uaculture practices. Animal welfare can be Global Sustainable Development Report guidelines for improving fish welfare [3] http://www.fishethogroup.net seen as one of these. identified animal welfare as a missing key in aquaculture worldwide (exception: (ASC) standard issue [9]. With this growing recognition of Once animals are kept in captivity to pro- the RSPCA guidelines for Atlantic [4] https://www.ccmar.ualg.pt/avanced- animal welfare as a critical issue in food duce food, farmers have an ethical respon- salmon and rainbow trout). The fair- tech-training/fish-welfare-course Janneke Aelen production, the inclusion of fish seems not sibility to provide them with acceptable, fish international association and its only relevant but necessary, given the rele- [5] https://www.asc-aqua.org/news/la ASC, Daalseplein 101, if not the best possible welfare conditions Fish Ethology and Welfare Group vance of aquaculture in current food pro- test-news/asc-responds-to-fish-welfare-re 3511 SX Utrecht, The Netherlands throughout their life cycle [1]. As other pro- (FishEthoGroup) were commissioned duction. Of course a strong scientific basis port/ – see also Janneke Aelen’s contri- [email protected] duction animals, fishes in captivity don’t by the Friend of the Sea (FOS) cer- is required to actually address fish welfare bution of on ‘Fish welfare indicators for the have the option to avoid or escape from tification scheme to develop fish wel- ASC standard’ in this issue Background ASC in a robust manner. fare criteria for the FOS standard. stressful events like aggressive conspecif- The Aquaculture Stewardship Council The Open Philanthropy Foundation ics, parasites or harmful environmental About 20 years ago fish welfare was a (ASC) is an independent non-profit organi- secured funding for the project. changes. Systems with a higher degree topic which was barely studied, but this sation that manages a stringent certification of intensification usually pose a higher risk has changed over the last two decades. The basis for the development of the and labelling programme for responsible for animal welfare issues. The advantage With thousands of papers being published guidelines was, on the one hand, the aquaculture based on species-specific of intensified systems is however that these on fish welfare, fundamental questions on scientific findings in the freely acces- standards. The ASC standards and certi- farmed species are under greater (environ- fish intelligence, stress and pain experi- sible online database FishEthoBase. fication guarantees to consumers that the mental) control which provides opportuni- ence are being answered and a founda- net set up by fair-fish for a growing seafood they are purchasing is sustainable ties to address and control potential wel- tion is being created for implementation number of species (currently 51) and, for the environment, and socially responsi- fare issues [2]. within legislation and welfare certification on the other hand, visits to FOS-certi- ble. The ASC was founded in 2010 by schemes [1] [2]. Examples of the progress Although animal welfare touches upon the fied fish farms. The first visit was for a the World Wide Fund for Nature (WWF) of fish welfare science are the handbooks three well-known pillars of sustainability gap analysis, with a report and sug- and the Dutch Sustainable Trade Initiative on welfare of Atlantic Salmon and Rainbow (economic, environmental and social), lo- gestions for improvement to the farm, (IDH). Trout, published as part of the FISHWELL cating the concept within one of these do- the second six months later to observe project by Nofima [10]. These elaborate The ASC is an example of multi-stakehold- mains has been complex [3]. Animal wel- which of the suggestions could be im- reports describe operational welfare indi- er governance, and a full member of the fare is sometimes placed under the social plemented and how, and which could cators for these two common aquaculture ISEAL Alliance, the global organisation for pillar as a social issue that needs to be met not, and why. Fifty-one fish farms species. The scientific knowledge is not as credible sustainability standards whose and animal health can sometimes be found from 33 companies in 12 countries advanced for all aquaculture species, but members must meet internationally accept- under the environmental pillar. Both animal with 26 fish species were visited. this is developing rapidly as gaps are be- ed best practice. Within its current ASC welfare and health can be seen as factors ing identified by different stakeholders and Conclusion after the first visit: the most species-specific standards, fish welfare is contributing to economical sustainability. research is focussing on practical imple- common problems concern lack of only partially addressed, and ASC has in For animal health the interlinkage with mentation in farming environments. fish welfare training of the staff, lack 2019 embarked on a Fish Welfare pro- environmental health and human health is of stunning before slaughter, stress of ject aimed at assessing how to expand widely proven and recognized within the Consumers seem willing to pay a premium the fish and lack of enrichment of the comprehensively the list of fish welfare- One Health concept [4]. Lesser known is for fish produced with an improved level of facilities with substrate and structures. related indicators and requirements in its the One Welfare [5] concept, highlighting welfare, but the availability of background Conclusion after the second visit: standards. the interconnections between animal wel- information and the timing of this informa- about half of the recommended im- fare, human wellbeing, and the environ- tion are key factors in the final consumer provements were under serious con- Animal welfare within ASC ment and emphasizing a holistic approach choice [11]. sideration or already implemented certification when addressing welfare related topics. after half a year. This adaptation per- This is exactly where (independent) labels The ASC standards originally have been This interlinkage between animal welfare play a vital role. Labels are a driver for con- formance of the farms shows that an structured around two major sustainability integration of fish welfare criteria into and other (sustainability) issues is increas- sumers when making ethical purchase deci- issues: environmental impact and condi- ingly being investigated and recognised. sions and information coming directly from the FOS certification standard is not tions of those working in in aquaculture unrealistic. For example, The EU and EFSA define it as the industry is often distrusted. Moreover, in- and communities that are directly affected an issue linked to food safety [6], and also formation on higher animal welfare can be The criteria and indicators developed by aquaculture practices. The aquaculture the FAO links animal welfare to food safety, a purchase motivation in itself, independ- by fair-fish are currently(August 2020) dialogues, initiated by WWF prioritized as well as to human and animal health, ent from the consumer level of empathy being prepared by FOS for its own these two aspects when developing the sustainability, and rural development. The towards animals, meaning that consumers standard and will then be submitted original ASC standards as they formed the targets of the UN Sustainable Develop- are sensitive to relevant information, rather major impacts from this industry. to the stakeholder process. Implemen- ment Goals (SDG) have been reviewed in that creating awareness is required [12]. tation is planned for 2021, with the Since its founding over ten years ago, compatibility with improving welfare, and So as long as animal welfare is not guaran- support of the FishEthoGroup, which ASC has been growing in size and ca- especially SDG 12, responsible consump- teed through other frameworks, food label- is now making its services in research, pacity, which allows the organisation to tion and production, and SDG 14, life un- ling adds value to the products and can be consultancy and training available to evaluate and expand its scope. This will der water, were found to have a mutually a motivation for consumers to shift towards Net cage brought ashore for repair from a Sea bass farm in Spain other stakeholders in aquaculture. beneficial relationship with animal welfare higher welfare animal products. (Photo: © Studer / fair-fish) inevitably lead to a more holistic approach

64 I FROM THE FIELD I 65 FROM THE FIELD

good welfare. Outcomes-based approach- be able to meet them and therefore should References The need for welfare labelling is especially and described as outdated. The freedoms al agreement among scientists is that fish es use minimal limits of (un)desired results. be carefully considered. The aspects of [1] Kristiansen T S, Bracke M B M, 2020. evident when legislation is lacking or is not are interconnected as some can be seen are conscious and experience emotions. They measure welfare in a more direct different production have to be taken into A Brief Look into the Origins of Fish unequivocal between countries. Fish have as a cause and effect of another, and it Numerous studies do confirm that fish have manner than resource-based indicators, account and there has to be a strategy in Welfare Science. In Kristiansen, T.S. et al. the status of sentient beings at EU level, is also not defined on what level they strong cognitive abilities as well. These are but there are potential practical challenges place for dealing with knowledge gaps on The Welfare of Fish (pp. 1-14). Cham: and are protected by EU Council Direc- should be met for good welfare to be ex- very strong reasons to accept that fish expe- for carrying out the measures. Continuous certain issues. Springer tive 98/58/EC concerning the protection perienced. The Five Freedoms also neglect rience welfare and that their welfare should improvement requires regular monitoring of of animals kept for farming purposes [13] the concept of positive welfare, whereas a be carefully assessed when being kept in certain criteria to ensure improvement and [2] Brown C, Dorey C, 2019. Pain and which states ‘to ensure the welfare of an- moderate state of hunger and thirst is not captivity for aquaculture practices. can be a direct driver for change. Compar- Take Home Message Emotion in Fishes – Fish Welfare Implica- imals under their care and to ensure that necessarily negative welfare. Finally, the ing different farms is likely to be challeng- tions for Fisheries and Aquaculture. Animal those animals are not caused any unnec- Five Freedoms framework lacks to reflect Animal welfare assessment ing using this approach, as the baseline Following the publication in Sep- Studies Journal, 8(2), 175-201 – see also an abbreviated version of their article in essary pain, suffering or injury’. At national systematically on cause and consequences The multidimensional aspect of animal (and level will vary between different farms. Ide- tember 2019 of an ASC Position this issue. level, the inclusion of fish welfare in legis- of the freedoms not being met, therefore the thus fish) welfare requires an approach of ally, in certification the three approaches Paper and of the Terms of Reference lation varies from none to very specific re- underlying cause of welfare issues may not complementary measures. There is no single are used in a complementary way [25]. of its Fish Welfare project [26], a [3] Buller H, Blokhuis H, Jensen P, Keeling quirements for example in Norwegian leg- be addressed when using these freedoms measure that can confirm good welfare or Technical Working Group (TWG) L, 2018. Towards Farm Animal Welfare islation. Globally, fish protection in national as a guideline [19] [20]. the absence of it. So welfare assessment Implementation was established in April 2020. and Sustainability. Animals 8(81). law is still the exception. relies on a range of indirect, reliable phys- within ASC certification in April 2020. It is composed of Then there is the question as to whether [4] One Health Initiative, 2021. https:// iological, biochemical and behavioural in- ASC has established a multi-stakeholder members from Academia, Uni- Given the fact that aquaculture products animal welfare can just be defined as the onehealthinitiative.com/ come from various regions in the world, absence of suffering. Most animal welfare dicators, reflecting all different dimensions Technical Working Group (TWG) for the versity, research institutions, NGOs, independent labelling seems like an ideal scientists believe there is more required of welfare [15] [23] [24]. Fish Welfare project with representatives fish farmers and other industry- [5] One Welfare, 2021. https://www. from academia, the aquaculture industry, related stakeholders (processors, etc). onewelfareworld.org/ option to provide consumers with aquacul- for welfare to be obtained [16] [19]. The As for any other standards, some common and NGO’s. As expertise is required on ASC has a very transparent process ture products where fish welfare is assessed possibility to experience positive welfare, ground rules ensure a framework of robust [6] EFSA, 2021. https://www.efsa.euro- various technical aspects and a range of regarding the selection of a broad in a credible way. or pleasure doesn’t have the same moral indicators. For this to be obtained, princi- pa.eu/en/topics/topic/animal-welfare species, the majority of the group exist range (sectoral, species-related and significance as avoiding suffering, but it ples used should be science-based, ethical- of technical experts from universities and regional) of key stakeholders related [7] Keeling L, Tunón H, Olmos Antillón G, Definition of animal welfare is a crucial condition to be able to speak ly valid, practical, and meet approval of veterinarians. This TWG will consider the to the topic to be discussed. Berg C, Jones M, Stuardo L, Swanson J, Animal welfare is a multidimensional con- about welfare. producers and public expectations [21]. scientific research available on the various Wallenbeck A, Winckler C, Blokhuis H, cept based on principles from veterinary Chosen measures also should be specific, The TWG has had several construc- Another determining factor of welfare is aspects of welfare issues in aquaculture 2019. Animal Welfare and the United sciences, ethology, ethics, endocrinology, valid, repeatable, and feasible [15] [22]. tive virtual meetings during which that all these negative and positive states systems. The fish welfare indicators will be Nations Sustainable Development Goals. and other fields [3] [14]. It contains as- In case of assessment as part of certifica- various aspects of fish welfare within are experienced on an individual basis on a species-specific level where needed. Frontiers in Veterinary Sciences. pects on a physical as well as a mental tion, assessment principles would be trans- aquaculture practices were discussed. [20]. Every sentient animal can have a dif- The developed content by the TWG will level [21], which makes it a very broad lated into standards and be supported by The outcomes of these discussions will [8] Cox J, Bridgers J. Why is Animal ferent experience of the same (environmen- go through two rounds of public consulta- field and impossible to measure directly elements of advice, inspection, certifica- be processed into draft indicators and Welfare Important for Sustainable Con- tal) situation and like all the other factors tion, where any stakeholder has a chance [15]. Another defining factor is that wel- tion, and accreditation. The certification will go through two rounds of public sumption and Production? UN Environment. and conditions, this has consequences for to provide feedback on this work. fare science in principle addresses animals scheme should meet certain conditions consultation. All stakeholders with an animal welfare assessment. [9] United Nations. He future is now – in captivity and how they cope with these like having an appropriate scope, practi- The first set of ASC welfare indicators will interest in fish welfare are invited to Science For Achieving Sustainable Devel- constrained conditions which is driven by a Probably the most controversial aspect of ani- cal focus, quality, transparency, effective form a base from where the fish welfare provide feedback on the draft content opment. Global Sustainable Development societal ethical concern [16]. mal welfare science is that it aims to measure communication, broad participation, and work can be developed during each 5-year developed by the TWG during these Report 2019. a subjective state of the animal, although it is reflection and improvement on its standards revision of the ASC standards. ASC aims to public consultation moments. The Frequently used interpretations of ani- widely accepted that animals have a qual- [25]. The inspection takes place as audits, play an active role in knowledge genera- first round of public consultation is [10] Noble C, Gismervik K, Iversen M H, mal welfare are the feeling-based, func- itative experience of life and are capable which should follow a structured plan, be tion and is part of partnerships addressing planned for September 2021. Kolarevic J, Nilsson J, Stien L H, Turnbull tion-based and nature-based definitions, of emotional suffering [21]. For animals to an independent and objective evaluation, specific knowledge gaps to make sure that J F. Welfare Indicators for farmed Atlantic where the feelings-based definition focuses The publication of the fish welfare in- experience a certain quality of life, species should assess the reliability and sufficiency new background information is available salmon: tools for assessing fish welfare. on the subjective state of the animal; the dicators within the ASC standards will should at least have neural structures which of provided information, assess the corre- for future revisions and implementation. Nofima,2018. function-based definition on the ability of form a solid baseline for fish welfare allow consciousness [1] [19]. spondence between claims and physical the animal to cope with its environment, Obviously, developing practical and audit- which ASC will be able to continue [11] Schelvis R, Steenbekkers B, Kole A, evidence, and communicates its findings in and the nature-based definition on the abil- Capabilities linked to this ‘emotional able welfare indicators comes with many to build on. Expected development of 2010. Diervriendelijk gekweekte vis: Wie a clear written report [21]. ity to express natural behaviour [17]. brain’ to experience welfare are experi- challenges. One has to consider auditabili- scientific knowledge and technologies wil dat betalen? Aquacultuur 8. ence, memories, re-evaluation of needs in Certification programmes can be based on ty, producer support, and consumer expec- that will keep advancing will progress Another well-known framework to describe [12] Cornish A C, Briley D, Wilson anticipation of physiological, psycholog- three different principles: tations in the process of indicator develop- fish welfare within aquaculture pro- animal welfare are the Five Freedoms, B J, Raubenheimer D, Schlosberg D, ical and behavioural requirements [22]. ment to be sure the standards are carried cesses and ASC is keen to play an drawn up by the FAWC. This framework 1. Resource-based; McGreevy P D, 2020. The price of good All of these mechanisms have a biological out correctly and are meaningful. Consum- active role in this field to move this as- uses five freedoms to describe desirable welfare: Does informing consumers about function to make animals able to learn from 2. Outcome-based; er knowledge and interpretation of com- pect of responsible production within states to address welfare. These five free- what on package labels mean for animal previous experience and avoid certain plex welfare issues may require accessible its standards. doms are freedom from hunger and thirst; 3. Continuous improvement. welfare influence their purchase intentions? negative experiences in the future by learn- information. Auditors and farmers will need discomfort; pain, injury or disease; fear Appetite 148. ing. So these qualities have to be identi- A resource-based approach describes re- training to get familiar with the aspects of and distress; and freedom to express nor- fied in fish to determine if the principles of quirements for welfare determining resourc- fish welfare in order to be able to carry out [13] https://eur-lex.europa.eu/legal- mal behaviour [18]. The Five Freedoms terrestrial animal welfare apply to fish. The es for the animal. Indicators taken from this what is asked of them. Increased produc- content/EN/TXT/?uri=CELEX- have been a reference for many assess- massive diversity in fish may make it difficult approach are easy to assess, but are insuf- tion costs as an effect of animal welfare :01998L0058-20191214 ment methodologies and are still often re- to prove this for all fish species, but gener- ficient on their own to draw conclusions on criteria can form a barrier for producers to ferred to. However, they are also criticized

66 I FROM THE FIELD I 67 FROM THE FIELD FROM THE FIELD

[14] Huntingford F, Kadri S, 2008. Wel- [19] Mellor D J, 2016. Updating Animal [24] Botreau R, Veissier I, Perny P, 2009. The purpose of this is that they can then • socially and ecologically sustainable fare and Fish. In: E.J. Branson (ed.) Fish Welfare Thinking: Moving beyond the Overall assessment of animal welfare: Tasks and working be appropriately applied to the production • easy to understand, uniformly Welfare (pp. 19–31). Oxford: Blackwell ‘Five Freedoms’ towards ‘A Life Worth strategy adopted in Welfare Quality®. of fish and other aquatic animals in other methods of the applicable, and simply formulated. Publishing. Living’. Animals 6(21). Animal Welfare 18: 363-370. ‘Aquaculture Welfare producing countries. Limits on the activities of the ITA: it is ex- [15] Blokhuis H, 2008. International co- [20] Webster J, 2016. Animal Welfare: [25] Main D C J, Mullan S, Atkinson C, New measures serving to improve animal Standards Initiative’ pressly not the ITA’s task to develop a new operation in animal welfare: the Welfare Freedoms, Dominions and ‘A Life Worth Cooper M, Wrathall J H M, Blokhuis H J, welfare in aquaculture animals based on certification or a new umbrella brand; Quality® Project. Acta Veterinaria Scandina- Living’. Animals 6(36). 2014. Best practice framework for animal scientific knowledge, which have not yet Stefan-Andreas Johnigk (dipl. biol.) rather, it is responsible for drafting a new via 50. welfare certification schemes.Trends in codified by the legislator, as well as the [21] Rushen J, Butterworth A, Swanson standard that is valid across the board as Food Science & Technology 37: 127– Initiativkreis Tierschutzstandards communication of particularly practicable [16] Duncan I J H, 2005. Science-based as- J C, 2011. Farm animal welfare assurance: guidance and a benchmark for the further 136. Aquakultur, methods for improving animal welfare in sessment of animal welfare: Farm animals. Science and application. Journal of Animal development of already-existing systems on Kieler Kuhle 3, the production process (‘best practice’) will Revue scientifique et technique (Interna- Science 89: 1219–1228. [26] https://www.asc-aqua.org/pro- the market. For the time being, the ITA will 24148 Wellingdorf, Germany also be incorporated into the ITA’s activities. tional Office of Epizootics) 24(2): gramme-improvements/fish-welfare/ not deal with animal welfare issues con- [22] Stien L H, Bracke M B M, Folkedal O, stefan.johnigk@aquaculture-welfare- 483–492. When developing recommendations, the cerning the catching of wild fish and ma- Nilsson J, Oppedal F, Torgersen T, Kittils- standards.net ITA uses the stage-gate process in innova- rine animals but will concentrate its work on [17] Fraser D, Weary D M, Pajor E A & en S, Midtlyng P J, Vindas M A, Øverli Ø, tion management. Aspects that are eligible issues relating to the breeding of fish and Milligan B N, 1997. A scientific concep- Kristiansen T S, 2013. Salmon Welfare In- Introduction for animal welfare improvements are exam- invertebrates. tion of animal welfare that reflects ethical dex Model (SWIM 1.0): a semantic model The breeding of fish and other aquatic ined to determine whether they are accept- concerns. Animal welfare, 6, 187–205. for overall welfare assessment of caged animals in aquaculture is attracting increas- The ITA is essentially open to all stakehold- able and feasible at all stages of the value Atlantic Salmon: review of the selected ing global attention year on year. Trade ers who make their own specialist contribu- [18] Farm Animal Welfare Council, chain. Only aspects that meet this initial welfare indicators and model presentation. in foodstuffs from this particular type of tions to the field of‘animal welfare and the National Archives, 2012. Five check can be considered as starting points Reviews in Aquaculture 5: 33–57. production has long been global and ex- sustainable aquaculture’ or want to imple- Freedoms. Available online: http:// for recommendations and are prioritised for tended across borders. At the same time, ment them in their field of work. The ITA webarchive.nationalarchives.gov. [23] Ashley P J, 2006. Fish welfare: Current processing. there are rising demands by society for the particularly encourages and strives for the uk/20121007104210/http://www. issues in aquaculture. Applied Animal Be- protection of these animals from avoidable All recommendations and criteria for an participation of experts with a focus on aq- fawc.org.uk/freedoms.htm haviour Science: 199–235. harm and suffering in many countries. animal welfare-friendly aquaculture that uaculture, animal welfare or animal health result from the work of the ITA are subject in the following areas: Due to inadequate international harmoni- to an ongoing improvement process. They sation of regulations on the protection of • Science and administration will be continuously further developed even the welfare of aquatic animals in aquacul- after their publication to enable long-term • Food retail ture up to this point, and a frequent lack sustainable improvement of the quality of of practical assistance, an initiative group • Fishing industry and aquaculture aquaculture. The ITA’s recommendations are of representatives from academia, animal enterprises initially to be considered as non-binding gui- breeding, business, public administration delines. They serve as guidance for mem- • Representatives from recognised and trade and animal welfare set up the bers of the ITA when reviewing and adapting subject-oriented NGOs ‘Aquaculture Welfare Standards Initiative’ their own guidelines (e.g. quality assurance (ITA) . In addition to producer associations, • Certification providers and certifiers measures in aquaculture production, procu- animal welfare and science, this group rement policy in food retail, adapting the The ITA operates internationally from Ger- already represents around 80 % of the guidelines of certification bodies, etc.). The many with the aim of including existing German food retail volume, along with the ITA does not have any influence or control and new initiatives from other countries and leading aquaculture certification bodies. over the way in which the recommendations achieving the broadest possible internation- al impact. Objective and procedure are implemented in practice. Members of the ITA acknowledge that their recommendations The ITA is aiming to instigate and lead an ITA membership is awarded on the invi- must be implemented in compliance with tation of the project coordinator and the industry-wide communication process for antitrust regulations and in consideration the development, drafting and implemen- signing of a letter of intent, a non-disclosure of market requirements for investments and agreement, and an antitrust law declara- tation of international animal welfare stand- innovation management. ards, irrespective of legal requirements. tion.

The ITA uses scientific knowledge, technical Requirements and strengths Method of negotiation developments, as well as social and legal of the ITA Unless otherwise agreed in the invitation to requirements for animal welfare-friendly aq- The animal welfare recommendations de- the meeting, German is the language used uaculture to develop recommendations for veloped by the ITA are for negotiations of the ITA. practicable international standards for the • scientifically sound breeding of fish and other aquatic organ- ITA members, who act as representatives of isms. The first step is to collate and evaluate • accepted across the industry a company or an organisation, ensure, to currently valid legal requirements for animal the best of their knowledge, that they have a • socially relevant welfare-friendly aquaculture in Germany mandate to negotiate the topics listed on the and other countries advanced in this field. • economically feasible agenda issued before each meeting. They View into a raceway with trouts (Photo: © Studer / fair-fish). 1 https://www.aquaculture-welfare-standards.net

68 I FROM THE FIELD I 69 FROM THE FIELD

undertake to treat each other with respect must be adequately considered. For examp- Intercultural communication of the most important aquaculture animal and to communicate in a spirit of mutual ap- le, not all stunning methods work equally as a challenge species, along with recommendations on Take Home Message stages of the value chain (innovation management based on the stage-gate preciation. It is in the common interest of all well on different species. There is a need The work of the ITA aims to make aqua- two issues included in the list of hotspots At the end of 2018, representatives model). Only aspects that pass this members to reach consensus on all issues to to specify more precisely the individual me- culture more animal-friendly worldwide. In considered to be relevant. from academia, animal breeding, initial check can be used as starting be decided, as far as this is possible, so that thods that can be regarded as appropriate contrast to existing standards (RSPCA, fair- With regard to the recruitment of suitable business, administration, trade, and points for recommendations. the greatest possible step is taken towards for ensuring and maintaining animal welfare. fish), the recommendations made by the ITA personnel (competent, multilingual, strong animal welfare founded the German achieving the ITA’s objectives. are not intended as a comprehensive draft As the needs of the fish — and conse- When selecting the animal species, the fol- communication skills), the initiative will have ‘Aquaculture Welfare Standards Initi- on animal welfare in aquaculture. Rather, it quently the measures required to im- What obligations do the members have? lowing should also be taken into account: to agree on alternative options for further ative’ (ITA). Around 80 % of the Ger- proposes that basic minimum requirements prove their welfare — differ between For the time being, there are no costs or their significance to food retail, the extent financing over the course of 2021, provided man food retail volume and the lead- should be defined which are globally ac- species, the recommendations are fees associated with taking part in the to which existing market certifications are that it appears to be desirable to continue the ing aquaculture certification bodies ‘Aquaculture Welfare Standards Initia- ceptable and implementable, regardless of specifically developed for individual available for them, and whether sufficient initiative’s activities beyond 2022. are also represented in this stakehold- tive’. For invited external experts and for expertise can be obtained from the ITA the country of origin and the type of culture. species. The plan is to develop recom- er group. The aim of the ITA is to insti- mendations for trout, carp, salmon, representatives of non-profit organisations, for scientifically based recommendations. The challenge will be to take into ac- References gate an industry-wide communication Gilthead seabream, Sea bass, Afri- travel expenses may be reimbursed by the To start with, research will concentrate count cultural differences concerning the [1] https://albertschweitzerfoundation. process in order to develop interna- can catfish, pikeperch, shrimp, tilapia, project coordinator upon request. The plan on species that are also produced in aq- importance attached to animal welfare is- org/campaigns/welfare-standards-aqua- tional animal welfare standards. The and pangasius. The ITA focuses on the is to organise a maximum of four joint face- uaculture in Germany. It can be assumed sues when communicating the objectives. culture-industry ITA develops recommendations for hotspots of stunning and slaughter, to-face events per year for ITA members. here that, for the purpose of deriving initial For example, the question of effective improving fish welfare on a scientific transport, handling, feeding, and Information is exchanged through e-mail recommendations, there is already a suffi- pre-slaughter stunning in German-speaking basis that is practice-oriented at the water quality. The plan is to over- correspondence, webinars, and online cient amount of data on good practice in countries is of great importance from the same time. These recommendations come intercultural differences in deal- meetings. accordance with applicable legal norms. consumers’ viewpoint. In contrast, in Medi- shall serve as guidance for ITA mem- In addition, species that are economically ing with animal welfare at product Supervisory body, specialist working groups: terranean countries, where the perishability bers for setting their own guidelines important and that are imported for Ger- quality level. currently there is no group hierarchy. of fish as a foodstuff is a significant concern and measures. When developing rec- man trade are to be selected. These are to the consumer due to the warmer climate, ommendations, the relevant aspects primarily: Why specific to individual fish pre-slaughter stunning is less of a priority for are checked to determine whether species? • Trout fish farmers. And in Asian producing coun- they are acceptable and feasible at all tries, for instance, far less importance is Each animal species has developed very • Carp attached to animal welfare than in the EU. special characteristics during its evolution in order to cope with the demands of the • Salmon In order to effectively level out such cul- environment. In animal breeding, these • Gilthead seabream tural differences, it is necessary to high- species-specific characteristics must be light the aspects of product quality, food • Sea bass adequately considered in order to avoid safety, and improved economic stabil- as far as possible any harm or suffering • African catfish ity that are associated with improve- caused by husbandry. ments in aquaculture animal welfare. • Pikeperch [See Table ‘Comparison of stakeholder In the case of terrestrial farm animals, expe- interests (stage-gate model)’ on p. 73 – 74] rience has been gathered from several mill- • Shrimp ennia of animal breeding and husbandry. In • Tilapia Future of the ITA—an outlook addition, agriculture focuses on a manage- • Pangasius ably small number of livestock species. In the The work of the ITA will become increas- case of aquatic animals, there is much less Order: trout and carp will be dealt with ingly international. Initially, the scope of ac- experience. Carp, for example, were not first, followed by salmon. Trout is ideal tivity will be expanded to include all Ger- adopted into pond culture until the Middle because there is already enough scientific man-speaking countries. After that, the ITA Ages; trout breeding was only developed in background information on the relevant ex- will have to agree on an expansion strate- the 19th century; and modern aquaculture isting hotspots and it is an important prod- gy into the rest of Europe that is compatible systems for salmon only draw on experience uct for the food retail sector. Furthermore, with the structure of the initiative. spanning the past few decades. there is an imbalance between the number Currently, most of the communication takes of trout products produced in accordance The number of fish species bred in aqua- place through direct face-to-face exchang- with German legal standards and the ac- culture around the world is far higher than es or in plenary sessions. This will no longer tual total number of trout products traded that of terrestrial animals; it has already be sustainable once the initiative reaches in Germany: according to estimates of the reached several hundreds of different spe- a critical size. At this point, the establish- German food retail industry, a good 80 % cies. Well-founded scientific knowledge on ment of smaller working teams, along with of trout is imported and it is far from cer- species-specific needs and peculiarities is a steering committee for quality assurance, tain whether production already meets the available for very few of these species. The will become an issue. animal welfare demands of German con- adoption of new species into aquaculture sumers. German aquaculture companies The ITA will be financed by project funds usually occurs through trial and error. view this situation as a market distortion. A from the Albert Schweitzer Foundation until When formulating animal welfare recom- harmonisation of the production standards 2022. The foundation expects the desired mendations, species-specific differences is desirable. (See Table ‘Which hotspots project results to include an agreement on Trout feeding (Photo: © Studer / fair-fish). does the ITA focus on?’ on p. 72) public recommendations for the stunning

70 I FROM THE FIELD I 71 FROM THE FIELD

Which hotspots does the ITA focus on? Comparison of stakeholder interests (stage-gate model) The recommendations made by the ITA will mainly focus on animal welfare aspects of the following key issues: When formulating minimum requirements for animal welfare in aquaculture, the demands and interests of the various stake- holders along the value chain must be adequately taken into account. If one aspect at a single stage of the chain encounters The practice of pre-slaughter stunning only plays a decisive role in the aquaculture rearing of aquatic disproportionately large hurdles in terms of implementation, its discussion will be postponed, and another animal welfare aspects animals within the last minutes of their life. However, from the consumers’ viewpoint, the topic of will become the focus of the ITA's work. Aspects that are deferred are not seen as less important for successful animal welfare. ‘killing’ plays an important role and needs to be dealt with accordingly with the necessary level of It is simply the case that their implementation depends on questions to which there are currently insufficient answers. The stake- sensitivity. The process of slaughter is pushed into the background. However, deficiencies in stunning holdergroups in the aquaculture value chain include all businesses and interest groups that can contribute to, or claim to improve, practice, or even the absence of any stunning before slaughter, create substantial potential for a animal welfare at their level. This may have to be weighted differently depending on the issue being addressed. Stunning and scandal and therefore represent a level of reputational risk for all parties involved in the aquaculture slaughter value chain that should not be underestimated. The issue is also suitable as a communicative bridge in dealing with producers from cultures in which animal welfare aspects receive less social attention The keeping of hatchlings (broodstock) gives rise to very specific issues from an animal welfare compared to within the EU. The avoidance of suffering and excessive stress during slaughter increases perspective. The extraction of germ cells through stripping and the use of genetically modified breeding lines are two examples that are currently attracting particular social attention. The water quality (free the product quality and shelf life to such an extent that these advantages can be used to formulate an Hatchery interculturally, easily understandable justification for effective stunning methods without the need to from specific pathogens), feeding (essential components, composition), careful handling, and emphasise ethical aspects. transportation (hygiene, survival rate) are among the ITA’s main topics of relevance to the production of fry/larvae. The transportation of stock and breeding animals is sometimes handled extremely differently in the producing countries, depending on their culture. The spectrum ranges from the use of a modern transport The production of juvenile fish for stocking fish farms often takes place outside the actual farms. tank with ventilation control to simple placement in an open basket. In addition to animal welfare-related Stocking fish The water quality (free of specific pathogens), handling, feeding (essential components, composition), Transportation effects of excessive stress, injuries to the animal and possible contamination with pathogens should be production and transportation (hygiene, survival rate) are among the ITA’s main topics of particular relevance to avoided as far as possible. As with the issue of stunning, there are numerous aspects that help to improve the production of juvenile fish. both the ethical and economic quality of production. The gentler the transport process, the lower the harmful effects on the animals transported and on their continued breeding. The issues of handling and transportation are particularly relevant to providers of commercial fish transportation between the various stages of production. The transportation of animals from aquaculture Fish transportation With regard to the handling of animals in aquaculture for necessary examinations such as vaccinations, is also handled very differently from a cultural perspective and is strongly linked to traditional images weighing, diagnosis, or when moving them to other areas of production, there is significant room for from the consumers’ viewpoint. improvement in terms of animal welfare. Stress, injuries and hygiene risks can be significantly reduced by using suitable methods or by avoiding unnecessary measures. Production type and economic All of the ITA’s main topics address specific aquaculture technology providers. For this sector, it should Handling be noted that the available technology must be suitable for both smaller extensive aquacultures and efficiency should factor into determining which animal-friendly handling methods can be implemented Technology larger units when it comes to scalability, technical requirements and required level of investment. A in practice. And in consumer communication, it is important to meet traditional expectations of ‘proper providers handling’ of fish by explaining in a sensitive manner that less stressful technical methods for handling collaboration with the ITA can be advantageous for technology providers if new incentives for product animals exist. improvement and product innovation can be derived from the recommendations made by the ITA.

When it comes to the issue of feeding, there is potential to improve animal welfare both in terms of feed In the production and composition of feed for animals in aquaculture, animal welfare-related matters arise that are only indirectly apparent to the producers. The issues of feeding and water quality are composition and feeding methodology. Animal feed represents a decisive cost factor in aquaculture. Feed producers Switching to supposedly cheaper feed could potentially not only cause loss of quality, it also involves particularly affected. Clear communication between the feed producer and the breeder is required in Feeding animal welfare risks. Overfeeding and underfeeding should be viewed equally critically. When the feed order to adequately resolve these issues. is presented, excessive feed competition, and its consequences for animal welfare, can be reduced by applying simple measures. All of the ITA’s main topics are important for operators of aquaculture facilities, provided that slaughter is also the farm’s responsibility. A particular challenge for the ITA is the fact that, depending on the type The water quality is, from the perspective of the animals cultivated in aquaculture, by far the most impor- and intensity of production, farms can use different control methods to implement improvements relevant tant welfare aspect. At the same time, this issue has the greatest need for scientific research and inves- Fish farmers to animal welfare. Extensive carp farming in traditional ponds poses different challenges compared to tigation. The impact of metabolites and feed residues on water quality, the introduction of oxygen, the intensive fish farming in closed circuit systems. The companies’ sizes enable problems to be solved using Water quality presence of pathogens and predators, as well as the temperature are influencing factors that are, in part, investment-rich methods to varying extents. And last but not least, very different knowledge management strongly interrelated. Depending on the type of culture and production intensity, there are also various and training requirements also apply across various forms of production. management strategies for maintaining sufficiently high water quality. It will be a challenge for the ITA to formulate recommendations on this issue that are simultaneously scientifically sound and practicable. If the slaughter of aquaculture animals is outsourced to an external company, animal welfare-related issues arise for the company, especially as they relate to pre-slaughter stunning, transportation and Food traders occasionally face demands by some animal welfare organisations to set upper limits on handling. Depending on the size of the company and its location, different technologies can be used to stocking density for the procurement of aquaculture products. The ITA will not make any recommendations Slaughterhouses solve these issues. on stocking density limits for the time being. Whether stocking density may lead to fish welfare problems For the ITA, it should be noted that existing technologies are not always adequately examined for their depends on a number of factors. Even in the case of extensive livestock farming with low stocking effectiveness with regard to animal welfare based on scientific data. Furthermore, slaughterhouse ins- densities, there can be a total loss of the population due to predators or adverse climatic conditions. And pection was not necessarily part of the previous certification practice of certification bodies. Stocking density within the same form of production, excellently managed farms with significantly higher stocking densities may comply better with animal welfare standards than those with serious deficiencies The processing of aquaculture animals is only linked to animal welfare issues in terms of the quality of in culture management. the products. Extreme stress during transportation, stunning, and slaughtering reduces the quality of the In addition, only a binding commitment by food traders to pay higher prices for aquacultural products meat. Obvious damage to the eyes, gills, skin, and fins make whole animal marketing difficult and also Cutting and produced in compliance with animal welfare standards would mean that producers did not have to involves reputational risks. processing compensate for the costs of animal welfare improvements by moderately increasing production. In this respect, processing companies certainly have their own vested interests in animal welfare improvements, but they can only be indirectly influenced through communication with their supplying producer/slaughterhouse.

72 I FROM THE FIELD I 73 FROM THE FIELD FROM THE FIELD

low margins for domestic aquaculture pro- As an intermediate level, this stakeholder group has so far been minimally active or inactive on the Coordination in ducts compared to imported goods. From issue of animal welfare in aquaculture. However, it could certainly be swayed by solutions from the ITA, Wholesalers the point of view of the trade, an improve- provided that appropriate offers for discussions are made by producers and retailers. The good Swiss aquaculture ment of the status quo of Swiss aquaculture reputation of aquaculture is in the very best interests of fish wholesalers. Thomas Janssens must therefore take place through a higher level of professionalisation along the entire Due to the interface function between producers, consumers, and market power, food retail is a main Bern University target for campaigns by NGOs. The reputational risk of all market participants is consistently high; value chain, with a resulting reduction in of Applied Sciences BFH-HAFL, a joint approach to reducing animal welfare problems is therefore in the interests of all companies in the production costs. Another solution would food retail trade. 3052 Zollikofen, Switzerland be to increase willingness to pay by pro- Food retail There are options for action that individual actors can take, both through internal specifications for [email protected] moting the image and better marketing of product procurement and the use of existing certificates. The Bern University of Applied Sciences ‘Swissness’. Fish welfare is seen as an im- For the ITA, it should be noted that the question of product quantities available on the market is just as (BFH-HAFL) and the Zurich University of portant aspect for consumers and produc- crucial as the need to make advertised animal welfare features verifiable on the product or in its tion in Switzerland. production. Applied Sciences (ZHAW) conducted a study with the aim of setting up a coordi- It is proposed that the tasks of a coordina- The various certification bodies for sustainably produced animal products from aquaculture are already nating office for Swiss aquaculture, i. e. for ting office should initially serve as broad a involved in incorporating animal welfare issues into their certificates. a very small sector that has grown strongly circle of users as possible. The creation of For the ITA, this results in the need to formulate recommendations for these stakeholders in such a way in recent years and is undergoing diver- an information portal and the coordination that they can be reflected in all existing certificates without endangering their independence as a brand. sification due to new types of production. of synergies should offer added value to It is primarily about harmonisation and the avoidance of contradictions in dealing with animal welfare This development phase brings uncertain- the sector. The visibility of Swiss aquacul- issues, as well as the avoidance of competition in this socially sensitive issue. Certification ties and challenges along the entire ture should be increased and the sector It should also be noted that certificates cannot be continuously amended but are subject to clearly bodies/Certifiers value chain, both for producers and for the should be helped to grow in an orderly regulated revision cycles. Recommendations made by the ITA must also be geared towards the ability to authorities. certify animal welfare – it must be measurable, countable, verifiable, or otherwise documented for a manner while complying with standards certifier at company level in a legally secure manner. In order to support the development of in animal welfare, environmental protec- A third aspect is that sustainability-oriented certificates are usually issued at the level of aquaculture Swiss aquaculture professionally in all tion, and product quality. The exchange farms. Upstream areas such as feed production or downstream areas such as slaughtering must be areas, the Federal Food Safety and Vete- with thematically related sectors should be recorded and mapped in a suitable manner at the same time. rinary Office(FSVO) intends to set up a strengthened. There is disagreement about coordinating office. Clarifications showed political representation. From the consumers’ viewpoint, the question arises as to how improved animal welfare conditions can great interest in such a body, but the ideas be identified when choosing aquaculture products. Studies show that end product labels do not achieve The coordinating body can be set up over regarding its tasks, financing and organisa- the desired broad impact; instead, they only appeal to a consistently narrow target group. In contrast, two years and in consultation with existing Consumers trust in the integrity of well-known brands and retail chains is a decisive factor for the successful marke- tion differ. The aim of this study is to create organisations. The role should be to co- ting of animal welfare-improved products. a basis for decision-making on the content, ordinate and support, not to take over or For the ITA, it is essential to communicate the adopted recommendations to consumers in such a way organisation, and staffing of the coordi- replace existing activities. The coordinating that the work of the ITA is perceived as both trustworthy and technically well-founded and relevant. nating office, and to define the necessary body should only act where necessary. Ini- steps. To this end, the current situation of tially, funding should come from the federal So far, the direct involvement of NGOs in the work of the ITA has been limited to the Albert Schweit- the aquaculture sector was examined. The government and gradually be replaced by zer Foundation’s campaign for welfare standards in the aquaculture industry [1]. The publicly raised NGOs information gathered was then used to as- membership fees and advisory manda- demands of other NGOs are continuously compared to the ITA’s hotspots, and active participation in sess the challenges of the development of tes. In the long term, federal contributions appropriate groups at EU level (Eurogroup for Animals, etc) is pursued as far as possible. the sector by various methods and to iden- should be limited to the operation of the tify and prioritise the tasks of a coordina- web portal and the preparation of an an- Official representatives who deal with animal welfare issues in aquaculture demand that all recommen- Official ting unit. A scenario analysis of possible nual sector report on aquaculture and its dations adopted by the ITA must be based on applicable law. veterinarians/ long-term developments and a proposal for For example, a recommendation by the ITA on stunning aquaculture animals may go further than the development. supervisory the next steps, including the financing of a legal requirements in the countries covered. However, as soon as a method is expressly not approved in authorities The report was finalised in September a target country, no such recommendation may be given by ITA. step-by-step implementation, conclude the study. 2020 and is now available [1]. The BFH- HAFL and the ZHAW have received a new There are numerous opportunities for the work of the ITA, starting from basic research on animal welfare The research revealed that a majority of the mandate from the FSVO for the next two issues in aquaculture to application-oriented research, the training of fish farmers, professional advice stakeholders interviewed consider the state years to create an information website, dis- and advanced training for breeders, and the veterinary care of breeding stocks. of the Swiss aquaculture sector to be unsa- Research/ An ITA recommendation should only be made based on sufficiently well-founded data. It does not tribute the tasks between the various play- tisfactory. There are many individual actors Science/ matter whether this is the results of scientific research, empirical experience from good practice or ers and find a long-term funding model. with their own goals, a high dependence Training/ the proprietary expertise of specialist advisors. It is crucial that the observations are reproducible and References Consulting transferable, and that they can withstand third-party testing. on production factors, synergies are hard- The ITA’s academic partners also play a decisive role in the transfer of knowledge for the successful ly used, information relevant to the sector [1] Report ‘Aufbau einer Koordinations- implementation of the ITA's recommendations. For example, publicly accessible course content can be is not accessible, production, processing, stelle für die Schweizer Aquakultur’ of made available in other languages; or the curriculum of existing courses can be expanded. and sales are highly isolated, and there are 5 March 2021, https://www.blv.admin. knowledge gaps in the planning and ope- ch/blv/de/home/tiere/tierschutz/nutz- ration of facilities. Together with the high tierhaltung.html price level in Switzerland, this results in high production costs. In addition, a lack of customs protection leads to comparatively

74 I FROM THE FIELD I 75 FROM THE FIELD

However, it soon became clear that it is and thus differentiation from foreign com- the Five Freedoms as defined by the Farm Intensive aquaculture precisely because of our vivid imagination petitors. We found what we were looking Animal Welfare Committee (FAWC) in as and animal welfare: that special caution is required when put- for in the areas of ‘resource efficiency’and early as 1993: ting such an idea into practice. In aqua- ‘animal welfare’, as Switzerland is an a practical example 1. freedom from hunger, thirst culture, the promising starting point all too international leader in both areas, both and malnutrition often tempts one to disregard the complex in terms of government regulation and in Georg O. Herriger and demanding aspects of sustainable fish terms of reality. 2. freedom from discomfort SWIFISH AG, farming. This is important for us at SWIFISH because 3. freedom from pain, Schachenweg 24, We at SWIFISH therefore set out on our ‘Swissness’ plays an important role not injury and disease 3250 Lyss, Switzerland journey quite consciously and only took only in exports, but also in the Swiss mar- [email protected] 4. freedom from fear and distress one step at a time. Since the begin- ket. A clear value positioning as a Swiss At the beginning, there was ‘only’ a mar- ning, it has been part of the DNA of the product is of central importance in the do- 5. freedom to express normal behaviour ket analysis for me: fish consumption is SWIFISH team to approach things care- mestic market, as this facilitates the accept- Crucial in this approach is to know or trendy — fish is light, healthy, modern. fully and prudently. There are no isolated ance of higher prices which compensate learn about the specific requirements of the Moreover, the current marginal domestic aspects to our approach – everything is for the higher Swiss production costs. In chosen fish species and to take them into share of about 2.5 % of Swiss consumption somehow connected. Nevertheless, I would short, since there is no customs protection account. (Figure 2). of seafood promises considerable growth like to try to focus on the issue of animal for fish, fish production without a Swissness Figure 2: Male pikeperch on the nest (Photo: © G. O. Herriger). potential for domestic fish production. From welfare and explain our goals and experi- premium would not be affordable or com- In our opinion, the choice to breed pike- an economic point of view, this sounds ences in this regard. petitive under Switzerland's cost structure. perch in closed recirculation systems is very tempting — also to me. justifiable. It is true that —like all fish —it is facilities must also be available … but in the so to speak — and has a corresponding As to the baseline on the market: animal Note: Respect for animal welfare as a a wild animal that has not or has hardly end, it is not the money that is decisive, but effect externally and internally. (Figure 4). After a series of clarifications and consid- welfare is increasingly playing a special pillar of willingness to pay in the market been domesticated and is kept in an artifi- the knowledge, the experience, and above erations, the noble fish pikeperch came role in the development of the ‘Swissness’ is an economic necessity for the reali- But let’s come back to the Five Freedoms cial environment. However, the pikeperch all the unconditional commitment of the into my focus. And so —together with brand concept today. The classic Swissness sation of fish production in Switzerland in animal welfare: thanks to the efforts of is a predatory species that does not roam team. This is the only way to ensure that the committed partners —I founded the SWIF- quality concept originally referred primari- that respects animal welfare. So much our team and the installations they have de- about but keeps still, lying in wait for its living conditions for the animals are always ISH company almost five years ago, with ly to the quality of products and services. for the economic boundary conditions. signed or optimised, we are able to satisfy prey, and is therefore not unsuitable for a optimal or at least acceptable —even in the aim of becoming a major supplier of However, the power of differentiation of (Figure1). the first four freedoms in an animal-friendly limited habitat in a recirculation system. the case of technical break- 100 % Swiss-bred pikeperch. Today, the these characteristics is constantly diminish- For us at SWIFISH, however, respect for an- After the first stages of development(fry/ downs, which happen all company owns a stocking facility in ing the better a comparable foreign quality imal welfare is not primarily an economic fingerling), it is not very aggressive towards the time. (Figure 3). Lyss (BE) and a RAS fattening facility for becomes. For this reason, efforts are being necessity, but an ethical one. We recognise conspecifics, which allows for largely prob- about 150 t of round fish per year, in- made to upgrade the term ‘Swissness’, I am also firmly convinced that we take on a special responsibility with lem-free schooling with appropriate and cluding its own processing installations in i. e. to supplement it with aspects that once that team spirit is the key suc- the rearing of the still barely domesticated controlled stocking densities. Susten (VS). again enable a credible positive distinction cess factor in highly sensitive wild animal pikeperch. We are guided by However, the pikeperch is extremely de- aquaculture. The SWIFISH manding in the fry and fingerling stage. team is characterised by a This includes the basic sensitivity of the lar- constant willingness to work vae and fry with regard to water quality, together in a thorough and light and temperature, the peculiarities in disciplined manner, to be the initial feeding (artemia) and develop- flexible and creative, to con- ment (swim bladder filling), all coupled stantly observe and learn, to with the tiny dimensions of the creatures. act as a community, and to And then there is cannibalism! Apparent- solve tricky problems (if nec- ly designed as a natural strategy for op- essary, with several sleepless timal feeding of the fittest, it is a constant nights …). So far, there are operational challenge for us with the need only a few such experienced for frequent size sorting. pikeperch specialists. SWIF- ISH is fortunate to have sev- The central challenges in terms of animal eral such experts in its team, welfare are congruent with the economic either as employees or as goals: we have to design the husbandry external consultants. conditions in such a way that as many in- dividuals as possible survive undamaged Every company has its and that no damage that impedes healthy own identity, which shapes further growth occurs. the overall behaviour and commitment of all persons In order to be really successful, the follow- involved. In the case of ing criterion applies to me: I need to be SWIFISH, it is the value of able to employ highly qualified and highly animal welfare that consti- motivated staff. Of course, the financial tutes the soul of the identity, means for the appropriate equipment of the Figure 1: Fingerling tanks in Lyss (BE) (Photo: © G. O. Herriger). Figure 3: Pikeperch eggs (Photo: © G. O. Herriger).

76 I FROM THE FIELD I 77 FROM THE FIELD FROM THE LIBRARY

SWIFISH gives preference to this natural This is in total contrast to the usual wild learning, cognition, and consciousness are This book is a print edition of the nine ar- way of reproducing on nests – in contrast catching of fish where fish would die cruelly The comprehensive new explored. Chapter 8 discusses awareness ticles published from 2018 and 2019 in to the common routine of using hormones, in nets, and which is analogous to the trap- book of fish welfare in fishes and other animals. In Chapter 9, a the Special Issue Welfare of Cultured and striping the pikeperch and hatching the ping of mammals. In terms of animal wel- novel way to look at how the brain works is Experimental Fishes of the open access eggs in jars. We find that this not only sat- fare, there is no greater contrast between Kristiansen T S, Fernö A, Pavlidis M A, presented. In Chapter 10, pain perception Fishes journal. The first chapter opens the isfies a special aspect of animal welfare, aquaculture and wild catch than in the way van de Vis H (Eds.), 2020. in fishes is discussed. Moreover, Chapter 11 book from the premise that the more evi- but also clears the way for ‘nature's intel- humans let the animals die! The Welfare of Fish. Springer Nature brings a new look at stress in fishes, where- dence about the mental capacities of fishes ligence’, resulting in eggs of high quality. as Chapter 12 reviews key components of in terms of behaviour, cognition, learning SWIFISH is still on its way to becoming Switzerland AG: Cham, We attribute this to the fact that the timing stress coping styles. and neuroscience grows, the more uncom- one of the leading Swiss suppliers of pike- Switzerland. 515 S. of egg maturation and natural mate selec- fortable the questions about fish welfare perch. To a certain extent, while ‘on the After this background about animal welfare, tion play an essential role in this. This book, which is part of a series on ani- and ethical implications become. This ope- way’ to this goal, a second objective has how fishes live and their capabilities, mal welfare, seeks to highlight the need to ning chapter highlights that although no Figure 4: Pikeperch larva In the last step — fattening — protection developed. This is namely, the manner in Chapter 13 explores in depth the question respect and improve fish welfare. The editors one usually wants to solve such questions, (Photo: © G. O. Herriger). against diseases is the top priority with which SWIFISH conducts aquaculture; it of how to assess the welfare state of these brought a large group of renowned resear- recent indicators show that this scenario is regard to animal welfare. Here, animal wants to set certain sustainability standards animals and the challenges involved. The chers who approach the welfare of these changing and that it is important to make welfare and economic objectives coincide in respect of fish welfare or, as it has been remaining chapters address specific issues way in terms of nutrition, husbandry, hand- animals from different angles, bringing a clear to the industry that once fish welfare once again. Since fish breathe in the same mandated since 1992 in Article 120 of about fish welfare related to the most diverse ling, and stress. With regard to the fifth very complete interdisciplinary view on the is improved, both the quality of the product medium in which they excrete, and since the Swiss Federal Constitution: to take into human actions and potential mitigation strate- freedom — the freedom to express normal topic, both in theoretical and practical ways. and its value increase. water is the same limited habitat for all an- account the dignity of the creature. gies. Thus, Chapter 14 addresses challenges behaviour — we have taken on a special, In the first part of the book, the readers are imals, any mistakes not only affect animal farmed fishes face; Chapter 15 investigates Thus, the following chapters of the book de facto unique challenge. presented the foundations of animal welfare, welfare, but also endanger the existence of ethical questions, and general aspects of problems with ornamental fish; Chapter 16 bring up diverse aspects related to fish This is where a species-specific peculiarity the entire stock. This is especially true for how fishes live, how their brain works and covers fishes used as laboratory animals; welfare, including health, growth, slaughte- of the pikeperch comes into play: that is, pikeperch with its high demand for oxygen, about their capabilities. These include be- Chapter 17 deals with commercial fish- ring, behavioural expressions and negative its extraordinarily complex reproductive be- its sensitivity to light and its generally low haviours, coping strategies, brain function, eries scenarios; Chapter 18 addresses and positive emotions, most of them clearly haviour, which we at SWIFISH classify not resistance to stress. Again, only an experi- stimuli perceptions and responses, cognition capture-based aquaculture combining indicating the importance to take these as- only as normal, but as essential behaviour enced team is able to provide optimal care abilities, and consciousness. In the second capture fisheries with aquaculture prac- pects into account also to assure better and and thus worthy of protection. for the welfare and growth of the animals, part, the book explores in depth the welfa- tices; Chapter 19 discusses problems with more profitable production systems. In this combined with strict hygiene. recreational fishing. Finally, Chapter 20 sense, although the chapters cover specific Pikeperch act in the mating season in a re issues, addressing each specific situati- reviews a question often ignored: the effects questions limited to the species investigated similar way to red deer: when the male A comprehensive view of the aspects of on involving human actions that affects fish of anthropogenic pollution on aquatic envi- in each paper, the scope of fish welfare is pikeperch senses spring, he looks for a nest animal welfare, however, leads us not welfare, since fish farming or lab conditions ronments for fishes. large, showing important findings of physi- and roars like a deer bull; the pikeperch is only from the egg to the mature fish, but to topics are often neglected, such as the cal, behavioural or emotional aspects. The the loudest freshwater fish! The intention is also to its optimal killing. In this respect, a impact of anthropic actions on the welfare Chapter 21 ends the book by bringing the book ends by discussing an online data- the same, namely to scare off competitors little-communicated but all the more signifi- of wild fishes. editors' view on fish welfare based on the base that provides scientifically based in- and attract females. These ‘test’ the offers cant advantage of aquaculture in relation previous chapters, summarizing important In this scenario, in Chapter 1, the authors formation about the welfare of farmed spe- and, depending on the situation, are ready to wild-caught fish becomes apparent: the aspects explored throughout the book, and revisit the origins of the animal welfare cies, bringing conclusions based on data for a mating dance in which they lay about avoidance of agony at death. In aquacul- highlighting that as fishes experience emo- movement, the various welfare definitions already available in such base. 100,000 eggs per kilogram of their own ture, the poikilothermic animals are kept in and how concern about domestic animals tions, their life should be made as pleasant body weight. The milter, the male, then has cool water for several days before slaugh- also gradually began to include fishes. In as possible. They also emphasize the need Chapters 2, 3 and 4 approach more phy- about 10 minutes to fertilise the eggs that ter, immobilised, then electrically anaesthe- Chapter 2, different theories of animal ethics for more scientific research about subjective sical aspects of fish welfare. In Chapter 2, quickly stick to the nest. He then guards the tised, and subsequently killed individually are introduced and ethical and moral issu- experiences, ranking different stressors, and the air exposition affecting the quality of the nest and fans the eggs with oxygen-rich by a gill cut. If carried out professionally, es are discussed. The following chapters the role of predictability and controllability meat of Catshark (Scyliorhinus canicular) water. The female is no longer involved in this is largely stress-free for the animals. show how fishes live, from an ecological aiming to focus on the gaps that most se- is approached, indicating that they should caring for the brood … (Figure 5). and behavioural approach, and how they verely limit the welfare of fishes. be rapidly slaughtered rather than die from asphyxiation. Chapter 3 brings the effect are shaped by the environment. Thus, Chap- Caroline Marques Maia ter 3 addresses the diverse world of fishes of phosphate fertilizers on growth, welfa- and how these animals have adapted to a re and product quality of African Catfish variety of habitats. In Chapter 4, the beha- (Clarias gariepinus), showing that low-level viour of fishes in the wild is explored and in Up-to-date overview phosphate fertilizers in the water can help Chapter 5, the authors examine the effects of fish welfare in plant growth in coupled aquaponics sys- of early life experience on behavioural de- aquaculture and tems without negatively affecting this fish. Chapter 4 investigates the influence of onto- velopment in captive fish species. The book animal testing follows by presenting what the fish brain is geny on the White seabream's (Diplodus like and how it works, besides discussing sargus) response to a common disease Arechavala-Lopez P, Saraiva J L (Eds.), the senses, responses and conscience of (Amyloodiniosis), showing that younger 2019 1. these animals. Chapter 6 give an overview fishes respond worse. of the anatomy, functionality, and evolution Welfare of Cultured and Experimental Chapters 5, 6 and 7 approach specific is- of the nervous system. In Chapter 7, fish Fishes. MDPI: Basel, Switzerland. 121 S. sues more related to behavioural aspects of Figure 5: Fattening tanks in Susten (VS) (Photo: © G. O. Herriger). 1 See also the article ‘Welfare of fishes — no longer the elephant in the room’ in this issue.

78 I FROM THE LIBRARY I 79 FROM THE LIBRARY FROM THE LIBRARY

fish welfare. Chapters 5 and 7 investigate In ‘Pleasurable Kingdom’ Balcombe, as a where melatonin, its biologically active me- expected. The authors highlight the presence Animal Welfare Act, the reluctance of local problems related to aggressive behaviours, recognised scientist, showed the courage Stress and fish welfare: tabolite and cortisol act together protecting of nociception mechanisms and related be- professional fishermen and fish farmers to a case of enrichment increasing aggres- to assemble many anecdotal observations indicators in the mucus the organism against unfavourable environ- havioural responses in these animals. The accept a label that promised them a higher siveness of zebrafish (Danio rerio) and on animals that are commonly frowned mental conditions, a local stress response definition of sentience is then revisited. Alt- price for special consideration for fish wel- a review covering common aquaculture upon as ‘not scientific’. In ‘What A Fish Magnoni L J, Martos-Sitcha J A, Prunet P, system in the skin. Ewa highlights that, alt- hough studies about animal cognition have fare and the environment, and the difficul- practices negatively affecting aggressive- Knows’, he also reproduces numerous an- Mancera J M, 2020. Welfare and hough dissimilarities of the stress response helped, there is no ‘practical’ definition of ties of creating a bridge for fairly caught ness of Nile tilapia (Oreochromis niloticus) ecdotes about observations of fishes that Stressors in Fish: Challenges Facing Aqua- systems of skin between fishes and terrestri- animal consciousness, but emotion-like sta- and paid fish to European retail chains in a and proposing practical ways to minimize were brought to his attention. In the book, culture. Lausanne: Frontiers Media SA. al vertebrates are expected, analysis of fish tes have been demonstrated in fishes, bees project lasting several years with artisanal it, respectively. In Chapter 6, the authors however, he clearly distinguishes between skin mucus, which is continuously secreted and other insects. Furthermore, examples of fishermen in Senegal. The fair-fish associ- address a behavioral expression related ‘scientific findings’, i. e. results that can be This is a Research Topic with 15 papers by cells and can be easily collected, con- studies demonstrating capacities of mental ation recognised that it was too small to to pain, thus linking negative behavioral reproduced by other scientists, for example published in the open access journal Fron- tains many components, being a source of representations and of thinking about one’s have a direct impact on the market and has and emotional aspects of fish welfare by from experiments, and ‘pre-scientific’ ob- tiers in Physiology in 2019. The opening information on the welfare status of farmed own actions towards these animals are since pursued campaigns instead of label showing reduced movement complexity in servations, because they are not repeated. editorial brings up controlled and monito- fishes. shown. projects to use public pressure to target zebrafishes when they feel pain. Finally, One of the strengths of the book is that this red environments as important to prevent stressful, suffering-causing practices in fishe- Ewa comments that metabolites such as In the final part, the authors propose a so- Chapter 8 is a review that brings up the separation of two levels of perception is fish stress in aquaculture production, which ries and aquaculture. glucose, lactate, protein, and cortisol in lution for the controversy from artificial in- need to also consider positive experiences not drawn in a judgmental way, but merely is in expansion. Stress may compromise fish skin mucus have already been studied to telligence, which shows complex learning In 2012, after several years of dispute with and emotions for fish welfare instead of just in a clarifying way. And rightly so; for if health and survival, a problem affecting the judge their suitability for determination of and motivational responses without subjec- the veterinary authorities about deficiencies focusing on preventing or reducing negati- science were shielded from random obser- economic success, public and scientists – physiological response to different stressors tive experience, and state that as absolute in the regulation and enforcement of fish ve aspects, which is common. vations, it would hardly come up with the as their awareness about fish welfare is and that a positive relation between stress scientific evidence of sentience is unlikely, welfare in aquaculture, the idea arose to idea of testing this or that hypothesis. This now increased – and ethical aspects of Chapter 9 ends the book by presenting markers in plasma and skin mucus was re- ‘sufficient uncertainty’ is enough to con- compile the widely scattered studies in would be all the more true for a science the use of fishes for aquaculture, research FishEthoBase, an online open access cently demonstrated. Thus, the author con- sider the species as worthy of welfare order to create an ethological profile for as young and widely ramified as that of and in fisheries. Then, the editorial unravels database that provides scientific informa- cludes that the analysis of cortisol together protection. They emphasize that a ‘lower each farmed fish species, which would al- fish behaviour, i. e. of well over 30,000 the next papers that address aspects about tion about behaviour and welfare of the with melatonin and its active metabolite degree’ of sentience does not mean less low the formulation of scientifically based species. understanding, assessing and minimizing farmed fish species, a reliable tool to as- stress response of fish. AFMK from the secreted mucus seems suffering and that classifying species based recommendations for improving fish wel- sess and improve welfare in aquaculture Balcombe first takes us on his own little bio- to be a promising approach to on-farm on how similar or emotionally important fare. The online database FishEthoBase, systems. Based on the already available graphy of dealing with fishes, from being The studies assess new aspects about stress assessment of fish welfare. they are to us to discuss sentience has no which Studer in turn launched as a sideline information on this database, the authors taken to school and going fishing, to his in rainbow trout (Oncorhynchus mykiss), scientific bases. The review ends highligh- after his retirement, developed in a few ye- Caroline Marques Maia conclude that the welfare status of farmed studies in biology and ethology, to the ger- Gilthead seabream (Sparus aurata), Sene- ting how we should focus less on debates ars into an innovative project with university fishes is still poor and that current fish far- mination of the inkling that fish are creatu- galese sole (Solea senegalensis), meagre of sentience and more on improving the life connections that now employs seven peo- ming technologies do not fully address res like us. He spent five years immersing (Argyrosomus regius) and European Sea of the animals under our care. ple with research and consulting in various welfare issues, but there is potential for im- himself in the world of fishes to write the bass (Dicentrarchus labrax), farmed fish countries and sets new standards – just at Improvement of life Caroline Marques Maia provement, which depends on researching book. He presents the different senses in species. There is a study about the role regardless of the degree the right time, as a growing number of fish of cortisol in exercise-enhanced growth in about species needs and also covering the fishes, including the lateral line, which we of sentience farmers are now also willing to pay more many remaining gaps. can only understand theoretically because zebrafish (Danio rerio) – a common lab attention to fish welfare. we do not experience anything similar, and animal, and another about acute stress in fair-fish: Caroline Marques Maia De Mori, B & Normando S, 2019. Billo Heinzpeter Studer he shows how the specific development of some species of octopuses after fish captu- Idea with impact a particular sense in a species is related to ring. The studies cover common potentially Is ‘History’ repeating itself? The case of fish the ecological niche that the species has stressful aspects of aquaculture as hypoxia, and arthropods’ sentience and welfare. Studer B H, 2020. managed to secure for itself in the course high density, temperature, diet problems, Ethics & Politics, 2: 491–516. About our relatives fair-fish — Because You Shouldn’t Tickle of evolution. handling, transport and vaccination. Many under water This review starts by pointing out that as Fishes, rueffer&rub, of them describe procedures that can de- there is no agreement on the definition of Thus, as one reads on, an incredible diver- crease negative effects, including a re- ISBN 978-3-906304-83-0 Balcombe J, 2018. sity of specific perceptual worlds becomes sentience, periodical debates about whe- view about essential oils as stress-reducing In the beginning it was just a small idea, apparent. Sometimes, in a passage, you ther a certain species could be conside- What A Fish Knows. Macmillan, New agents. Some studies show indicators to a leisure activity, so to speak, recalls Billo find yourself involuntarily asking the ques- red as sentient and thus deservers welfare York. 2016. ISBN 978-0-374-28821-1. assess stress response, as biomarkers and Heinzpeter Studer in his recently published tion: what is it actually like for me? How considerations occur. The authors highlight a device monitoring the frequency of phy- book about the history of fair-fish from The North American ethologist Jonathan do I perceive this or that – and what re- that these tend to end with most researchers sical and respiratory activity once attached his personal perspective. In 1997, while Balcombe has become well known to mains hidden for me because I lack the recognizing sentience in the species or ad- to the operculum. still managing director of the Swiss farm a wider audience since his book ‘Pleasur- sharpened sense for it? Balcombe's book vising to consider it for precaution and that animal protection organisation KAGfrei- able Kingdom’1 was published. His book is not only a great introduction to the life Ewa Kulczykowska’s paper brings up an the debate then moves to a species less si- land, he had begun to develop guidelines ‘What A Fish Knows’ is in no way inferior. of fishes, it is also an invitation to wonder interesting proposal to complement the milar to humans, repeating the cycle. They for animal- and environmentally friendly fish In 304 pages, the author takes us across about life itself and its many forms. I wish evaluation of welfare of farmed fishes. The go through fishes and, more recently, arth- farms and fisheries on the side. In 2000, all kinds of fish species and shows an for this book many readers who will not put approach suggests the cutaneous stress re- ropods debates bringing them up as good together with several animal protection incredible variety of abilities of seeing, it down until they have read the last page sponse system (CSRS) as a new source of examples of such repetitions. organisations, he founded the association hearing, smelling, feeling, up to amazing and who will then perceive the world with information about fish welfare. The author Sentience of fishes and arthropods is then fair-fish with the aim of creating publicity for cognitive performances of our ‘underwater a little more reverence and love. highlights that its research group has shown discussed. Although they lack the neocortex, the then still exotic concern of fish welfare, relatives’. the basic conditions for the functioning of which is involved in human conscious awa- Billo Heinzpeter Studer one of the first such organisations world- a CSRS in fishes similarly as in mammals, reness, different structures evolving to per- wide. The author describes the success Spawning pond of an organic carp farm form the same function in different animals is 1 Palgrave MacMillan, 2007, ISBN 978-1-403986023 in the course of the revision of the Swiss in Austria (Photo: © Studer / fair-fish).

80 I FROM THE LIBRARY I 81 ON ANIMAL WELFARE LAW / FROM THE JURISDICTION ON ANIMAL WELFARE LAW / FROM THE JURISDICTION

(Art. 288 para. 3, TFEU). This means that However, the provisions of the Animal • European Convention on the Protection appropriate methods. Fishes are not ex- designated by the respective canton with- Fishes in animal welfare the directives must be transposed into na- Welfare Slaughter Ordinance do not of Animals during International Trans- plicitly mentioned in this convention, but out further prerequisites, such as a fishing law in Europe tional law by the EU member states. apply to mass capture if, according to port of 6 November 2003: According do fall under the definition of animals. licence or similar (cf. for example, § 3 of the state of scientific knowledge, stunning to Art. 2, this convention applies to the the Law on Fishing of the Canton of Zurich Animal welfare law Switzerland Antoine F. Goetschel 1 (Dr.), would not be possible or would only be international transport of all vertebrate of 5 December 1976 LS 923.1). More in the European Union Andrea Kellenberger 2 (MLaw) possible with disproportionate effort. animals, which means that fishes are Animal welfare has had constitutional detailed information, such as the permit- also included. Accordingly, the objective ted fishing methods, etc., can be found in According to the Treaty of Lisbon, animal Since the EU framework law does not con- status in Switzerland since 1973 and is Global Animal Law GAL Association, of the convention is, as various articles the respective cantonal fisheries laws. In welfare is part of the EU's remit. The EU tain any concrete regulations regarding stun- enshrined in Art. 80 of the Swiss Federal Witikonerstrasse 30, agree, to protect animals from injury, the light of general animal welfare legis- sees itself as an economic community ning, slaughter, and killing of fish, concrete Constitution. The confederation is obliged 8032 Zurich, Switzerland pain or suffering and to ensure their safety lation, cantonal free fishing rights should and only regulates animal welfare issues requirements can only be enacted within the to regulate the protection and welfare of 1 during transport (cf. Art. 6 ff.). be viewed critically. In the past, criminal [email protected] if they have economic or trade policy im- framework of the respective national laws animals in a binding and uniform manner 2 offences have repeatedly been found in [email protected] plications. With the Treaty of Lisbon of 1 of the member states (see the example of • European Convention for the Protection for the whole of Switzerland. The two most which the accused free anglers did not kill December 2009, the EU and its member Germany above). However, many member of Animals kept for Farming Purposes of important enactments in Swiss animal This article aims to provide a brief over- the animals they caught in a proper and states committed themselves to pay full re- states do not have any corresponding animal 10 March 1976: This convention is also welfare law are the Animal Welfare Act view of the relevant sources and standards professional manner (cf. criminal cases da- gard to the welfare requirements of animals welfare regulations. EU-wide harmonisation applicable to fishes bred or kept for the (AWA) and the Animal Welfare Ordinance for the protection of fishes in the European tabase of the Foundation for Animals in the as sentient beings in all policies relating to would be desirable here. production of food (cf. Art. 1). Art. 2 states (AWO). The AWA is what is called frame- Union (EU), Switzerland and Norway. In Law). The sometimes inadequate expertise agriculture, fisheries, transport, the inter- that the principles of animal welfare set work law that regulates the legal treatment addition, a brief introduction to the rele- The rules for the welfare of farm animals in of free fishermen in dealing with fishes with nal market, research, and technological out in the articles must be applied by each of animals in general. The corresponding vant European structures will be given. An- the EU are laid down in Council Directive regard to animal welfare legislation con- development and space (Art. 13, TFEU). party. These include, for example, con- detailed regulations are then found in the imal welfare law is understood to be the 98/58/EC concerning the protection of tains a correspondingly large potential for Through the explicit inclusion in the above- sideration of the stage of development, AWO. These federal provisions take pre- totality of all legislative legal norms which animals kept for farming purposes. Fishes possible cruelty to animals within the mean- mentioned provision, the member states are adaptation and domestication as well as cedence over any cantonal provisions in primarily pursue the goal of regulating the are explicitly mentioned in the directive ac- ing of Art. 26 et seq., AWA. accordingly obliged, not only in agriculture the physiological and ethological needs this area (Art. 49 para. 1 of the Federal behaviour of humans towards animals and cording to Art. 2, but only Art. 3 is appli- but also in fisheries, to take into full account of the animals or fishes. The convention Constitution). The principle of ‘federal law prevent them from inflicting unjustified pain, cable to them. This states that EU member the welfare of fishes as sentient beings. thus aims to ensure that all animals kept breaks cantonal law’ applies. This means suffering or harm or otherwise disregarding states are obliged to ensure that owners for farming purposes are not subjected that the cantons are only entitled to enforce their dignity. In the field of secondary legislation, the or keepers take all reasonable measures Box to unnecessary suffering or harm during federal animal protection law and to issue Council of the European Union has adopt- to safeguard the welfare of the animals in husbandry, feeding and care. corresponding implementing provisions. Overview of the legal structures ed Regulation (EC) No. 1099/2009 of their care and to ensure that no unneces- Excursus: Animal welfare of the European Union 24 September 2009 on the protection of sary pain, suffering or injury is inflicted on • European Convention for the Protection Swiss animal welfare law is based on the and the Common Fisheries EU law is divided into primary and second- animals at the time of slaughter. Art. 1 these animals. Art. 4 sets out further require- of Pet Animals of 13 November 1987: guiding principle of regulating the behav- Policy (CFP) in the EU. of this regulation mentions that only the re- iour of humans towards animals and estab- ary law. Primary law is the highest-ranking ments for the conditions under which ani- Pets are animals which humans keep for A major problem for the health of the quirements laid down in Art. 3(1) apply to lishing provisions for their protection and law of the EU. It consists mainly of the mals are kept, however, fishes are explicitly their own pleasure and as companions, seas and their inhabitants is overfishing fishes and that the regulation does not ap- welfare accordingly. In the scope of the An- founding treaties and the other amend- excluded. especially in their households, or animals in the EU's marine areas. Overfishing ply to recreational fisheries. Art. 3(1) states imal Welfare Act, Art. 2 para. 1 states that ing treaties, accession treaties and sup- which are intended for this purpose. Ac- means that more fish are caught than that during killing and related activities, Council Regulation (EC) No 1/2005 of this provision applies to vertebrate animals. plementary treaties. In terms of content, cordingly, fishes are also covered by this can naturally grow back. On the one animals should be spared any avoidable 22 December 2004 on the protection It is well known that fishes are vertebrates, primary law determines the distribution of convention. According to Art. 3, no one hand, high catches of fish are desirable pain, stress, and suffering. Each Member of animals during transport and related which is why they also fall within the scope powers and responsibilities between the may cause unnecessary pain or suffering for member states, but on the other hand, State is allowed to enact regulations that operations does not mention fishes, but as of the AWA. In addition, further animal pro- EU and its member states. For animal wel- to pet animals or induce them to have the ability of fish stocks to reproduce go beyond the minimum requirements. Ger- they are vertebrate animals, the transport tection principles can be found under the fare laws in the area of European prima- fear or abandon them. must not be impaired. According to many, for example, has made use of this of fishes must be carried out in accordance margin heading Principles’ in Art. 4 of the ry law, the Treaty of Lisbon is particularly Art. 38 of the TFEU, the EU pursues provision and issued the Animal Welfare with the regulation. The general rules for • European Convention for the Protection AWA. According to paragraph 2 of this worth mentioning. The legal provisions a common agricultural and fisheries Slaughter Ordinance. In addition to the re- transport therefore apply to fishes. The gen- of Vertebrate Animals used for Experi- provision, no one may unjustifiably inflict (regulations, directives, decisions, recom- policy. The Common Fisheries Policy quirements for the stunning and slaughter eral transport regulations are not appropri- mental and other Scientific Purposes of pain, suffering or harm on an animal, in- mendations and opinions) based on the (CFP) is regulated by Regulation (EU) or killing of vertebrates, crustaceans or mol- ate for fishes, as they were mainly created 18 March 1986 (with Appendices): This duce an animal to have fear or otherwise principles and objectives of the above- No. 1380/2013. The aim is to ensure luscs, this also contains regulations for the for land animals. convention applies to all animals used disregard an animal’s dignity. Likewise, the mentioned treaties are referred to as the long-term environmental, social, and storage of fishes and crustaceans before or intended for use in experiments or mistreatment, neglect or unnecessary over- secondary law. economic sustainability of fisheries and slaughter. The stunning, slaughter and kill- Council of Europe Conventions other scientific procedures where such exertion of animals is prohibited by law. aquaculture activities. The objectives Regulations are rules which are directly ing of fishes and crustaceans is regulated on the Protection of Animals procedures may cause pain, suffering, The provisions of the Federal Act on Fish- of the CFP are to be achieved through applicable in a member state (Art. 288 in § 12. Accordingly, in addition to the re- The Council of Europe has also drawn up distress or lasting harm. An animal under eries (FAF) in particular are reserved for the multiannual plans, technical measures, para. 2 of the Treaty on the Functioning quirements under EU law, animals must be five conventions on the protection of ani- this convention, is defined as any living scope of the AWA. Notably, this law out- and the setting and allocation of maxi- of the European Union [TFEU]). Directives, stunned in such a way that they are brought mals. These conventions are international vertebrate other than a human being. In lines the principles according to which the mum allowable fishing. From an animal on the other hand, set out an objective quickly and without pain or suffering to a treaties that must be ratified in order to be particular, for fishes, Art. 3.8.5 mentions cantons must regulate and control fishing welfare point of view, Regulation No. to be achieved, but it is up to the indi- state of sensory deprivation and insensi- binding. They only regulate minimum stand- that tolerance to acid, chlorine and many for fish and crayfish. The Federal Council 1380/2013 of the CFP makes it clear vidual member states to enact their bility that lasts until death. ards, which was the consensus reached by other chemicals varies greatly from spe- issues the implementing provisions, while in paragraph 16 of the preamble that own legislation to achieve the objective the contracting nations. cies to species. the respective cantons are responsible for full account must be taken of animal • European Convention for the Protection enforcement (Art. 21, FAF). health and welfare requirements. This is of Animals for Slaughter of 10 May done in implementation of the principles 1 In principle, GAL follows the idea of ‘One Health’: it requires healthy humans and healthy animals to live together in order Many cantons in Switzerland have what 1979: Art. 12 states that animals shall, of Art. 13 of the TFEU as primary law to ultimately bring about a recovery of the Earth system. Worldwide, about 2/3 of all infectious diseases originate from animals, are called free fishing rights. This is under- if necessary, be restrained immediately mentioned in the article. including COVID-19. before slaughter and anaesthetised by stood as the right to fish in certain waters

82 I ON ANIMAL WELFARE LAW / FROM THE JURISDICTION I 83 ON ANIMAL WELFARE LAW / FROM THE JURISDICTION

Norway Deutscher Tierschutzbund, Töten von Niedersächsisches Amt für Verbraucher- Box Take Home Message Swiss animal protection law, which is Norway protects animals through its own Fischen aus Aquakulturen, Bonn 2015. schutz und Lebensmittelsicherheit, Be- the only one to date that also recog- täubung und Schlachtung oder Tötung von Animal Welfare Act (Lov om dyre-velferd Errass Ch: Tierschutz. In Ehrenzeller B, Excursus: Fishing in Norway Most of the animal welfare legislation nises the dignity of animals as worthy Fischen, Rechtsgrundlagen und deren prak- of 19 June 2009). According to Section 1, Schindler B, Schweizer R J, und Vallender The EU has concluded a ‘Northern in Europe today applies to terrestri- of protection, has also expressly ap- tische Umsetzung. the aim of this Act is to promote animal K A. (Hrsg.), Die schweizerische Bundes- Fisheries Agreement’ with Norway. al vertebrates, and fishes are only plied to fishes since 2008, irrespective welfare and respect for animals. The scope verfassung. St. Galler Kommentar. Zürich, Regulation (EU) 2019/1022 of the Euro- On the one hand, this fisheries agree- protected in very general terms. For of the way in which they are used. The of the Act, according to Section 2, also St. Gallen 2014, S. 1614 mit Hinweisen. pean Parliament and of the Council of 20 ment regulates the joint management fishes in aquaculture, their capacity to regulations for farmed fishes are sim- explicitly extends to fishes. Section 14 also June 2019 establishing a multiannual plan of stocks with the aim of sustainable suffer is taken into account to some ilar to those in Germany. The require- EU legislation, https://europa.eu/europe- mentions that it is prohibited to use violence for the fisheries exploiting demersal stocks fishing, and on the other, it is intend- extent, whereas in fisheries, the provi- ment to immediately stun and kill wild an-union/law_en against animals, to place animals in a help- in the western Mediterranean Sea and ed to regulate the exchange of fishing sions focus on species protection, not fishes caught is, with exceptions, not less condition, to have sexual intercourse European Council, 10 February 2020, amending Regulation (EU) No 508/2014, quotas and access to the exclusive animal welfare. applicable to commercial fisheries. with animals or to perform sexual acts on Management of the EU's fish stocks, https://eur-lex.europa.eu/legal-content/ economic zones of each party. The them, or to use live animals as food or bait. The EU animal welfare regulations Multiannual management plans, https:// EN/TXT/PDF/?uri=CELEX:32019R1022 fisheries agreement with Norway is Fishing shall be carried out in compliance also cover fishes, though are limit- www.consilium.europa.eu/en/poli- the most comprehensive in Northern Schärmeli L, Griffel A, 2015: Tier- with the Act (§ 20). The penal provisions ed to general requirements, such as cies/eu-fish-stocks/multiannual-manage- Europe. The main issues discussed in Literature schutz. In: Waldmann B, Belser E M, are contained in § 37, and in the case of the requirement that fishes should ment-plans/ Animal Welfare Act, Switzerland, serious violations of this law, a prison sen- the annual consultations are the set- also be spared any avoidable pain, und Epiney A (Hrsg.) Bundesver- https://www.fedlex.admin.ch/eli/ European Commission, The Common tence of up to three years is possible. The ting of maximum catch levels (T&Cs stress and suffering during slaughter. fassung. Basler Kommentar. Basel cc/2008/414/en Fisheries Policy (CFP): Managing fisheries, European Convention for the Protection of for cod, plaice and haddock) for the However, prior stunning is left entire- 2015, S. 1347 – 1348. jointly managed stocks in the North https://ec.europa.eu/fisheries/cfp/fish- Animals during International Transport, the ly to national legislation and is only Animal Welfare Ordinance, Switzer- Special Report of the European Court of Sea and the exchange of fishing op- ing_rules_en. European Convention for the Protection of required by a few member states. land, https://www.fedlex.admin.ch/eli/ Auditors, No 31/2018: Animal welfare portunities. Animals kept for Farming Purposes, the Eu- Germany, for example, requires stun- oc/2018/173/de Ferrari A, Goetschel A F, Heiglauer M, in the EU: closing the gap between ambi- ropean Convention for the Protection of Pet ning before slaughter in aquaculture, Kellenberger A, und Oertly D, 2019. tious goals and practical implementation, Fishing vessels flying the flag of Nor- Bolliger G, 2000. Europäisches Tierschutz- Animals, the European Convention for the but not in fisheries where it is not GAL Kantons-Vollzugs-Kompass 1.0, https://op.europa.eu/webpub/eca/spe- way may fish in EU waters within the recht, Tierschutzbestimmungen des Europa- Protection of Vertebrate Animals used for possible or reasonable according to Zürich 2019, S. 19. cial-reports/animal-welfare-31-2018/en/ T&Cs set out in Annex I to Council rats und der Europäischen Union (mit einer Experimental and other Scientific Purposes, Regulation (EU) 2020/123 of 27 current science to carry out stunning ergänzenden Darstellung des schweizeri- Fisheries Agreement with Norway: Tierschutz in der Europäischen Union, and the European Convention for the Pro- January 2020, fixing for 2020 the in mass capture. With regard to the schen Rechts), Zürich 2000, S. 21 ff. https://ec.europa.eu/fisheries/cfp/inter- Albert Schweitzer Stiftung für unsere Mit- tection of Animals for Slaughter have also fishing opportunities for certain fish living conditions of farmed fishes, the national/agreements/norway. welt, 20. Juli 2012. been ratified by Norway into national leg- stocks and groups of fish stocks, ap- EU also limits itself to the general pro- Bolliger G, Goetschel A F, Richner M, und islation. Regulation (EC) No. 1099/2009 plicable in EU waters and, for EU ves- vision that all reasonable measures Spring A, 2008. Tier im Recht Transparent, Giménez-Candela M, Saraiva J L, and of 24 September 2009 on the protection sels, in certain non-EU waters and are must be taken to ensure the welfare of Zürich 2008, S. 6, 15, 401–402. Bauer H, 2020. The legal protection of animals at the time of killing does not ap- the animals and their protection from of farmed fish in Europe – analysing the subject to the conditions laid down in Bundesamt für Lebensmittelsicherheit und ply to Norway, as Norway is not a mem- unnecessary pain, suffering or injury. range of EU legislation and the impact of this Regulation and in Title III of Regu- Veterinärwesen, Illegale Fischerei (IUU), ber state of the EU. Specific provisions are again left to international animal welfare standards for lation (EU) 2017/2403. Bern 18. Dezember 2018. the member states. the fishes in European aquaculture. Dere- Currently, the Royal Ministry of Trade Bundesministerium für Ernährung und cho Animal (Forum of Animal Law Stud- The Council of Europe's five animal and Fisheries is considering new reg- Landwirtschaft, Internationale Fischerei, ies) 11/1 (2020). – DOI https://doi. welfare conventions have also done ulations for angling tourism. In the fu- Fischereiabkommen der EU mit Drittstaaten org/10.5565/rev/da.460 little for fishes so far. The Convention ture, only anglers who have registered vom 9. August 2019. their holiday in registered tourist es- for the Protection of Animals kept for Goetschel A F, 1986. Kommentar zum Eid- tablishments will be allowed to export Farming Purposes, which also re- Council of the EU, Press release, 6 June genössischen Tierschutzgesetz, Bern, Stutt- fish from the country, and: quires that the development, adapta- 2019: First ever multi-annual manage- gart 1986, S. 22–28. tion and domestication stages, as well ment plan for fisheries in the Western Goetschel A F, und Bolliger G, 2003. Das • Holidaymakers will only be allowed as the physiological and ethological Mediterranean becomes reality, https:// Tier im Recht, 99 Facetten der Mensch-Tier- to take 20 kg of whole, gutted and needs of fishes, be taken into account, www.consilium.europa.eu/en/press/ Beziehung von A bis Z, Zürich 2003, S. headed fish (instead of the previous goes somewhat further than the EU. press-releases/2019/06/06/first-ev- 46–49, 51–53, 58–61. 10kg of fish fillets). Here too, however, the detailed reg- er-multi-annual-management-plan-for-fish- • The export quota is to be increased ulations are left to the will of the indi- eries-in-the-western-mediterranean-be- Hirt A, Maisack C, und Moritz J, 2016. from seven days to one year. vidual contracting states. comes-reality/ Tierschutzgesetz mit TierSch-HundeV, TierSchNutztV, TierSchVersV, EU-Tiertrans- Council of the EU, Press release, 12 Decem- The reasons for the changes are mainly port-VO, TierSchlV, EU-Tierschlacht-VO, ber 2018: Multiannual management plan sustainability and transparency. Kommentar, 3. Aufl. München 2016, S. for Western Waters: provisional agreement 26–27, 421, 499–502. confirmed by the Council,https://www. consilium.europa.eu/en/press/press-re- HØring-Forslag til endring av regler om leases/2018/12/12/multiannual-man- turistfiske, HØring 6. Januar 2020; Euro- agement-plan-for-western-waters-provision- päischer Rat, Bewirtschaftung der Fischbe- al-agreement-confirmed-by-the-council/ stände, Internationale Fischereiabkommen, Brüssel 19. Dezember 2018.

84 I ON ANIMAL WELFARE LAW / FROM THE JURISDICTION I 85 ON ANIMAL WELFARE LAW / FROM THE JURISDICTION

punishment of animal welfare offences brates, fall within the scope of the Swiss At present, the commercial breeding and Deficits in the enforcement welfare offences committed against fishes. The fish in Swiss law — committed against fish by the criminal Animal Welfare Act. However, if one com- farming of fishes for human consumption of animal welfare offences Of these, 27 cases concerned ornamental current criminal cases authorities. pares the legal regulations concerning the and restocking purposes is only rudimen- committed against fishes fishes and 67 cases the handling of fish- husbandry and handling of fishes with tho- tarily regulated. As already mentioned, Animal welfare offences are punished on es for human consumption [17]. In view The moral status of fishes Christine Künzli (MLaw) se concerning other farm, pet or laboratory specific husbandry and management re- the basis of the criminal offences laid down of these low numbers of cases, it can be Current research provides a differentiated animals—given their wide biological ran- gulations for individual fish species exist in the Animal Welfare Act (AWA) and can assumed that there is a high number of Stiftung für das Tier im Recht picture of the fish which strongly deviates ge—the handling of fishes is regulated in only for salmonids and cpriniformes, largely be divided into the two main cate- unreported cases of animal welfare offenc- (TIR, Foundation for the Animal in the Law), from the common notion that it is a mute, a significantly less species-specific manner. although in practice more and more new gories of ‘cruelty to animals’ and ‘other es that are not prosecuted and punished Rigistrasse 9, 8006 Zurich, Switzerland fish species are being farmed in Switzer- [10, p. 44 et seq]. insentient creature. It is scientifically un- Any person handling fishes must take their offences’. The offences of ‘mistreatment’, [email protected] land, such as perch, pikeperch, tilapia, disputed that fishes are sentient animals. needs into account in the best possible way ‘neglect’, ‘unnecessary over-exertion’, In the last 16 years, the most common of- and sturgeon [14]. Humans use fishes in a variety of ways. Accordingly, they are covered by ani- and ensure their welfare (Art. 4 lit. a and b ‘disregard for dignity in other ways’, fence in the criminal decisions dealing with They are fished for food, kept as orna- mal welfare legislation (Art. 2 AWA [1]). AWA [1]). In addition, no one may unjusti- From an animal welfare point of view, the ‘painful or wanton killing’, ‘organisa- violations against fishes has been fishing mental fish in aquaria, bred in aquaculture However, the capability of fishes to feel fiably cause pain, suffering or harm to a exceptions to the ban on the use of barbed tion of cruel animal fights’, ‘carrying out with barbed hooks. Other offences which for food production and used in animal pain is still a matter of dispute among fish, induce anxiety or otherwise disregard hooks and live bait fish, as well as to the avoidable animal experiments’ and the were focussed on were the failure to carry experiments to gain scientific knowledge. scientists. Some experts doubt that fishes its dignity (Art. 4 para. 2 AWA). Further- principle that caught fishes must be killed ‘release or abandonment of animals’, as out an immediate kill, other cruel killing Fishes are living creatures capable of suf- have the neurological prerequisites to feel more, the general provisions of the Animal immediately (Art. 23 para. 2 OWA [2]), defined inArt. 26 AWA [1], qualify as cru- methods, mistreatment and violations of fering and feeling. As vertebrates, they are pain at all [6] (see for example the article Welfare Ordinance (AWO [2]) must be ob- are to be criticised in particular. These ex- elty to animals. Violations under this article, the keeping conditions. This ratio is also covered by Swiss animal protection law in by Lynne Sneddon [9] on this issue). The served when handling fishes, in particular ceptions are regulated in the Ordinance to if committed intentionally, are punishable confirmed for the criminal decisions issued the same way as, for example, dogs, cats, question of the ability of fish to feel pain Art. 3 to 16. For example, fishes must be the Federal Law on Fisheries (VBGF [3]). by imprisonment of up to three years or in 2018 [17]. If criminal proceedings are birds or cattle. Accordingly, the principle is legally relevant and has implications for kept in such a way that their bodily func- Another major animal welfare problem is a fine. If the offender acts negligently, a initiated for offences committed against that the welfare and dignity of animals must animal welfare regulations regarding their tions and behaviour are not disturbed and the exception in Art. 97 para. 3 OWA, ac- fine not exceeding 180 daily penalty units fish, then these are relatively often serious be protected (Art. 1 of the Swiss Animal husbandry and killing. Based on the lat- their adaptability is not overtaxed (Art. 3 cording to which the catching and killing (Art. 26 para. 2 AWA) is to be imposed. offences. Welfare Act, AWA [1]) also applies to est scientific findings, it can be assumed para. 1 AWO [2]). Table 7 of Annex 2 of of fishes is permitted without a certificate The offences of cruelty to animals are thus The use of barbed hooks in particular caus- them. It is therefore forbidden, among other that fish do not simply react reflexively to the Animal Welfare Ordinance lists mini- of competence for fishing in public waters misdemeanours according to Art. 10 para. es considerable pain to the fish and ac- things, to unjustifiably inflict pain, suffering pain stimuli, but that they have the physi- mum requirements for stocking density and if the canton concerned does not require 3 of the Swiss Criminal Code, SCC [4]. or harm on fish, to induce anxiety in them, cal and mental prerequisites to consciously cordingly constitutes mistreatment within the water quality for the keeping and transport a patent or a short patent of up to one All other violations of animal welfare law, to humiliate them, to instrumentalise them perceive pain and to suffer as a result [7, meaning of Art. 26 para. 1 lit. a AWA. In of salmonids and cypriniforms only. With month's duration. This regulation leads on the other hand, are referred to as oth- excessively or to interfere profoundly with p. 52ff, 156ff] [8| [9| [13]. For the ma- 2018, 47 proceedings were carried out regard to the keeping of ornamental fish, to the fact that in most cantons fishing is er offences within the meaning of Art. 28 their appearance or capabilities (Art. 3 lit. jority of the ECNH members, scientific due to the use of barbs. However, the ca- Table 7 of Annex 2 (AWO [2]) sets out cer- also allowed without training. It can be AWA [1]. These are offences under Art. a AWA [1]). evidence does not provide proof of the suistry proves that the competent authorities tain minimum requirements for the size and assumed that the lack of training of many 103 SCC [4], punishable by a fine of sentience of fishes. However, the circum- still sometimes underestimate the capacity Nevertheless, the legal protection of fishes equipment of aquaria. For example, they hobby fishermen results in a high number up to 20,000 Swiss francs. Negligence, stantial evidence makes it difficult to deny of fishes to suffer and classify the use of is insufficient in many respects. Similarly, must prevent direct visibility from all sides, of catches and killings that do not comply instigation, aiding and abetting and at least certain fish species the ability to barbs as a violation of the animal pro- the annual analysis of Swiss animal welfare and parts of the aquarium must provide pri- with animal protection regulations [10, p. attempt as defined in Art. 28 para. 2 feel pain. Moreover, in view of the com- tection regulations (Art. 28 para. 1 lit. a law enforcement by the Stiftung für das Tier vacy and refuge for the fishes. 43]. The exceptions mentioned can lead AWA are punishable by a fine of up to plexity of the phenomenon ‘pain’, the AWA) — and thus merely as a contraven- im Recht (TIR, Foundation for the Animal in to considerable suffering for the animals 10,000 Swiss francs (Art. 106 SCC). scientific findings to date are not sufficient In view of the biological range of creatures tion and not as cruelty to animals, which the Law) shows that offences against fishes concerned and are an impressive example When applying the above-mentioned of- to fundamentally deny fishes the ability to that are called fish, the general keeping ultimately leads to a considerably lower are still not prosecuted by the competent of the fact that the legislator does not take fences, it must always be checked wheth- feel pain. A minority of the commission and handling regulations in the Animal sanction [10, p. 49] [17]. In the same year, law enforcement authorities. Accordingly, adequately into account the fact that fishes er an act to be judged already fulfils the members were even of the opinion that, Protection Ordinance are insufficient. Ac- 22 cases were brought against fishermen an enormous number of unreported cas- are sentient beings, capable of suffering requirements of an offence of cruelty based on the scientific findings, a form of cording to current scientific knowledge, who failed to kill a fish intended for con- es of animal welfare offences committed and experiencing pain, that also have a to animals according to Art. 26 AWA. pain perception must be attested to fishes about half of the estimated 64,000 verteb- sumption immediately and professionally. against fishes can be assumed. Both the legally recognised dignity. If this is the case, its application is man- [5, p. 17]. rate species are fishes [5, p. 7]. The great In the context of this offence variant, it is current animal welfare regulations and the diversity of species and the different needs The scientific confirmation of fishes' abili- datory. Art. 28 AWA thus represents also evident that the competent prosecution criminal practice in connection with animal Based on current scientific findings, it is of the animals are in no way taken into ty to feel pain must lead to a fundamental a kind of catch-all offence for less se- authorities still do not draw the line be- welfare offences committed against fishes therefore quite plausible to assume that account by the existing regulations. For change in thinking in society and politics rious interventions that nevertheless af- tween the individual offences defined by do not by far come up to the current state fish can feel pain. Accordingly, fish are to example, Art. 98 AWO (keeping of fishes and ultimately to stricter animal welfare fect the dignity and welfare of animals the Animal Welfare Act with sufficient pre- of knowledge regarding their sensitivity be attributed a moral status (intrinsic value) and crayfishes) only deals with water quali- regulations with regard to all forms of hus- in a way that is contrary to criminal law cision. For example, the Zurich Municipal and cognitive abilities. The Federal Ethics independent of their benefit to humanity ty and does not contain any further provisi- bandry and handling of fish — whether in [11, p. 18 et seq]. Office sentenced a defendant who mere- Committee on Nonhuman Biotechnology and the effects of the globally increasing ons on relevant keeping criteria such as sto- aquaristics, aquaculture, commercial fish- Although several million aquarium fishes ly stunned a fish with a blow to the head (ECNH) states in its ‘Ethical Treatment of fish consumption on the environment. This cking density, composition of the animals, ing, recreational fishing, breeding or in the of various species are kept in Switzerland after catching it and then placing it in a Fishes’ report that the moral status of fishes circumstance has been reflected in animal available space, infrastructure, feeding, context of animal experiments. The ECNH [12] [15], professional and angling fisher- plastic bag on the basis of Art. 28 Para. 1 has been discussed to a much lesser extent protection legislation in recent years, but light, noise or social contacts. Likewise, the is also of the opinion that the latest scientific men together achieve a catch of around lit. f AWA (unlawful slaughter), although in jurisprudence than in the case of other only insufficiently. legislator has failed to react to the ongoing findings on fishes must have consequences 2,000 tonnes of fish per year and profes- the more serious offence of Art. 26 Para. 1 vertebrates [5, page 3]. aquaculture trend. The fact that more and for human interaction with them: stunning AWA (cruelty to animals) was undoubtedly Inadequate legal coverage sional fish farms produce an additional The following is an overview of the current more fishes are being used as livestock for and killing methods as well as husbandry 1,500 tonnes of fish[16] , the criminal au- committed. The incorrect stunning and kill- The inadequacy of the ethical discussion on scientific discussion on the ability of fish food production must be taken into account conditions in breeding, research, private thorities deal relatively rarely with animal ing of the fish led to considerable suffering the moral status of fishes is reflected in the to feel pain, the insufficient coverage of at the legal level by enacting appropriate husbandry and fishing must be reviewed welfare offences committed against fishes: [17, cases ZH18/172 and VD17/0]. degree of differentiation of the legal regu- husbandry and handling regulations—for [5, p. 23ff]. this issue by Swiss animal welfare legisla- in 2018, only 94 criminal proceedings Similarly, it is still difficult for the compe- lations: It is true that fishes, like other verte- example on stocking density or feeding. tion, and the inadequate prosecution and were conducted in Switzerland for animal tent prosecuting authorities to distinguish

86 I ON ANIMAL WELFARE LAW / FROM THE JURISDICTION I 87 ON ANIMAL WELFARE LAW / FROM THE JURISDICTION

between poor husbandry (Art. 28 para. 1 Still trivialised References [11] Bolliger G, Richner M, Rüttimann A, Take Home Message lit. a AWA) and neglect or maltreatment The above examples show that offences Legal enactments Stohner N, 2019. Schweizer Tierschutzstraf- (Art. 26 para. 1 lit. a AWA): an animal is against fishes are still trivialised by the com- [1] Animal Welfare Act (AWA) of 16 recht in Theorie und Praxis, Schriften zum Fishes are still often regarded by socie- neglected within the meaning of Art. 26 petent law enforcement authorities. This Dezember 2005, https://www.fedlex.ad- Tier im Recht, Band 1, 2 Auflage, Zürich, ty, lawmakers and law enforcement para. 1 lit. a AWA if its owner or carer ex- finding is also borne out by the fact that the min.ch/eli/cc/2008/414/en Basel, Genf 2019. agencies as creatures without a sense poses it to the risk that its welfare could be penalties imposed for animal welfare vio- of pain. However, this perception does [2] Animal Welfare Ordinance (AWI) of [12] STS 2019, Tierschutzprobleme in der impaired due to inadequate care (includ- lations committed against fishes are often not correspond to the current state of 23 April 2008, https://www.fedlex.ad- Schweizer Zierfischhaltung,Schweizer ing inadequate medical care), nutrition, very mild and the available range of pen- science, which recognises the ability min.ch/eli/oc/2018/173/d Tierschutz STS, Basel 2019. accommodation, activities or exercise op- alties is far from exhausted [10, p. 53ff]. portunities [11, p. 129ff]. In contrast, any of fishes to suffer and feel pain as This is the case even when Art. 26 AWA [3] Federal Law on Fisheries of 21 June Websites plausible. The current animal welfare behaviour that causes an animal pain, is correctly applied: the public prosecutor's 1991, https://www.fedlex.admin.ch/ regulations as well as the casuistry of [13] fischwissen.ch, last visited 30 March suffering, harm or distress of a certain office in Zurich, for example, sentenced a eli/cc/1991/2259_2259_2259/ animal welfare offences committed 2020. significance is considered mistreatment defendant to a conditional fine of 15 daily de – Ordinance of 24 November 1993, against fishes show that both politics [11, p. 120f]. The offence of Art. 28 penalty units of 180 Swiss francs each https://www.fedlex.admin.ch/eli/ [14] Schweiz. Fischereiveband, sfv-fsp.ch, and the responsible authorities lack para. 1 lit. a AWA only applies if the of- for failing to clean his aquarium, change cc/1993/3384_3384_3384/de last visited 30 March 2020. sufficient sensitivity to the needs of fence in question is of an absolutely minor the water and replace the broken oxygen fishes. The Swiss Animal Welfare Act [4] Swiss Criminal Code (SCC) of 21 De- [15] Verband für Heimtiernahrung, vhn. nature [11, p. 129ff]. The public prose- pump, so that the fishes suffered in the con- regulates the keeping and handling of cember 1937, https://www.fedlex.ad- ch, last visited 30 March 2020. cutor's office in St Gallen sentenced a de- taminated water and two animals died in fishes only rudimentarily and not in a min.ch/eli/cc/54/757_781_799/en fendant who had not cleaned his aquarium agony due to the lack of oxygen [17, Case [16] Bundesamt für Statistik, bfs.admin. way that reflects the considerable di- for seven months and had seriously neglect- ZH18/218]. The Pfäffikon governor's of- ch, Tabelle „Produktion und Konsum von versity of species. In addition, animal Literature ed the water quality, only on the basis of fice sentenced a defendant who first kept Fisch”, last visited 30 March 2020. welfare offences committed against [5| EKAH 2014. Bericht der Eidgenössis- Art. 28 para. 1 lit. a AWA. This is despite 27 caught fishes in a closed bucket in the fishes are still trivialised by the pros- che Ethikkommission für die Biotechnologie [17] TIR database of criminal cases, www. the fact that it can be assumed that the in- sun and then killed the animals without pri- ecuting authorities. A more in-depth im Ausserhumanbereich „Ethischer Um- tierimrecht.org/de/tierschutzstraffaelle sufficient water quality severely impaired or stunning to a fine of 500 francs [17, examination by science, society, poli- gang mit Fischen”, Dezember 2014, Seite the welfare of the fish concerned, which case ZH16/343]. The public prosecutor's tics, and law enforcement agencies of 3, https://www.ekah.admin.ch/de/me- is why the offence of neglect according to office of the Emmental-Oberaargau region the pain perception of fishes and the dienmitteilungen-und-veranstaltungen/me- Art. 26 Para. 1 lit. a AWA should have sentenced a defendant who did not supply related animal welfare problems is dienmitteilungen/uebersicht/archiv/ethis- been applied [17, Case SG18/100]. In eight fishes with sufficient oxygen and did indispensable for the increased pro- cher-umgang-mit-fischen-dezember-2014/ this context, reference should also be made not ensure that they could not jump out of tection of fishes. to the decision of the public prosecutor's of- the basin to a conditional fine of five daily [6] Key B, 2016. Why fish do not feel fice of the Bern-Mittelland region in 2015, penalty units of 100 francs each. Seven fish pain. Animal Sentience 3(1). in which a defendant who kept piranhas died and one fish swam ‘barely breath- [7] Wild M, 2012. Fische. Kognition, and ornamental fish in the same aquarium, ing’ on the surface of the water during the Bewusstsein und Schmerz – eine philoso- which led to them being attacked and in- authorities’ check [17, case BE17/200]. jured, failed to provide medical care and phische Perspektive, in: Eidgenössische was wrongly convicted on the basis of Ethikkommission für die Biotechnologie im Art. 28 para. 1 lit. a AWA and not on Ausserhumanbereich EKAH und Ariane the grounds of cruelty to animals [17, case Willemsen (Hrsg.), Beiträge zur Ethik und BE15/176]. The public prosecutor's office Biotechnologie, Band 10, Bern 2012. in Solothurn also convicted a defendant of Seiten 52ff. und 156ff. a simple violation of the husbandry regula- [8] Segner H, 2012. Fish. Nociception tions, even though dead fishes were float- and pain. A biological perspective. In: Ei- ing among the live animals in his heavily dgenössische Ethikkommission für die Bio- polluted aquarium [17, case SO13/022]. technologie im Ausserhumanbereich EKAH In recent years, there have also been an in- und Ariane Willemsen (Hrsg.), Beiträge zur creasing number of convictions for mistreat- Ethik und Biotechnologie, Band 9, Bern ment or agonising killing of fishes caused 2012. by the pollution of watercourses. [9] Sneddon L, 2019. Evolution of nocice- In addition to the provisions of the Water ption and pain: evidence from fish models. Protection Act, animal welfare regulations Philos Trans R Soc Lond B Biol Sci 374, must always be examined in such cases: 20190290. if the water pollution causes pain, suffer- [10] Flückiger N, Künzli Ch, Rüttimann ing, harm or distress to the affected fish, A, Richner M, 2014. Schweizer Tier- the offence of mistreatment pursuant to Art. schutzstrafpraxis 2013 mit besonderer 26 para. 1 lit. a AWA is fulfilled. If the Berücksichtigung der an Fischen begange- animals die as a result of the pollution, the nen Tierschutzverstösse, November 2014. offence of agonising killing pursuant to Art. Seite 23. 26 para. 1 lit. b AWA must be examined.

88 I ON ANIMAL WELFARE LAW / FROM THE JURISDICTION I 89 FROM THE IGN

successful keeping of undocked animals in you should take advantage of it. In my thusiasm for them is not necessarily shared We would like to thank Interview with our conventional pig houses is a great chal- opinion, if things don’t go as planned, it’s by others. Unlike a puppy dog or a chicken Dr. Dorian Patzkéwitsch an IGN member lenge. There is still a long way to go, but I not the end of the world (or the paper). chick, a juvenile fish probably evokes few for the interview. am optimistic. heightened emotions in most people. While What is your motivation for your they may not be the primary trigger of va- What brought you to your field? work? rious animal welfare debates, fishes can To be honest, it was more of a coincidence Since I started my career, I have been certainly benefit from the general discussion than a destiny. In my opinion, the omni- dealing with animal welfare issues in the around animal welfare in the coming years. presence of dogs, cats and horses in veter- field of farm animals. Two topics that are For its part, the increasing research into pain inary medicine studies is still very much in particularly close to my heart are the gesta- perception in fish is also making an impor- evidence today. Accordingly, pigs played tion crate housing of sows and the use of tant contribution. Aquaculture (against the a rather subordinate role for me (I actual- occupational materials for pigs. Both areas background of overfishing of the oceans) ly always wanted to go into the field of are now gaining momentum with the plan- will also become increasingly important exotics …). After my studies in 2013, ned amendment of the German Farm Animal in the future. Consumers are already de- however, I was offered the chance to work Welfare Ordinance. Even though these are manding more precise information on the on a project at the Ludwig Maximilian small steps with partly long transition peri- labels of fish products. As you can see, the University (LMU) in Munich that dealt with ods, things are nevertheless moving forward. topic of fish welfare is present and will most pig keeping. Through direct collaboration, likely become even more of a focus in the I learned to appreciate pigs very quickly. Which current developments do coming years. You simply have to like pigs. you find good/bad? My private interest, however, is mainly in Animal welfare, animal protection and fishes. Even if it's not my main focus, I'm animal-friendly husbandry are all terms that always pleased when I find professional have found their way into everyday life and interfaces in this thoroughly exotic field. society more and more in recent years. Even To be honest, to this day I can't walk along a if the meaning of these words is often not stream, river or lake without peering into the questioned further, one notices that the om- water at least once in the hope of spotting nipresent interest in these topics has strongly a scaled animal. This fascination is difficult increased. This is one of the reasons why to explain, but it has been strong in me from one or another supposedly deadlocked dis- an early age. cussion can still be brought up again, which Dr. Dorian Patzkéwitsch for me is a positive development. Who was your most important Specialist veterinarian mentor and why? What comes to your mind when for animal welfare, you think of IGN? Staatliches Veterinäramt, I would like to dedicate this answer to my Even if only indirectly, I had contact with Landratsamt Rosenheim, former boss Prof. Dr. Dr. Michael Erhard. the IGN relatively early on. In my literature 83022 Rosenheim, Germany Through the exciting work during his profes- sorship at LMU Munich, I was able to get research, I have always come across one [email protected] involved in many different areas and thus IGN booklet or another, which has always develop professionally. Without Michael's helped me in my respective tasks. For this What are you most involved open and tolerant manner and leadership, reason, it is also a great honour for me to with at the moment? this would not have been possible. My time be able to contribute to the current issue. My current professional focus is on the at university with him as professor and boss I immediately associate the IGN with the abandonment of tail docking in pigs. I am has had a great impact on me. unique international conference of applied involved in the technical implementation of ethology in Freiburg. The IGN award cer- the National Action Plan for the Discontinu- What advice would you give emonies in particular were a highlight for ation of Culling in Bavaria at the LGL. It is to a young colleague? me every time. It is always exciting to learn also one of my tasks to support the various If I may give some advice (I am still relatively about the different research results of other groups of people (including livestock own- young myself), I would say that it is important institutions. Of course, this event is also a ers, veterinarians and the authorities) in the to be open to everything, especially at the great opportunity to meet and exchange practical implementation of this. beginning of your professional life. There ideas with many great colleagues (espe- The routine docking of pigs' tails has been are many exciting, but also important, cially those from Austria and Switzerland). banned in the EU for a long time. Unfortu- topics to work on that you might not have nately, the reality is somewhat different. If thought of during your studies. What importance do you think fish welfare will have in ten you look around at conventional pig prac- It is of great value if you are given a certain years' time? tice, you quickly realise that the majority of amount of creative freedom, particularly animals are docked or kept docked. There if you are a young, enthusiastic research Fishes will always hold a certain special are many causes for tail biting, and so the place in my heart. I often notice that my en- assistant. So if you get such an opportunity, (Photo: © V. Patzkéwitsch).

90 I FROM THE IGN I 91 NOTES NOTES

92 I FROM THE IGN I 93 NOTES NOTES

94 I FROM THE IGN I 95 INTERNATIONALE GESELLSCHAFT FÜR NUTZTIERHALTUNG SOCIÉTÉ INTERNATIONALE POUR LA GARDE DES ANIMAUX DE FERME INTERNATIONAL SOCIETY OF LIVESTOCK HUSBANDRY

Imprint Information brochure of the IGN e.V. about current results from research on animal welfare.

Editor Billo Heinzpeter Studer: President fair-fish international association, Guarantor Fish Ethology and Welfare Group, Via delle Giarrette 109, Marina Julia, 34074 Monfalcone, Italy E-mail: [email protected] Reviewer: Johanna Moritz, Bayerisches Landesamt für Gesundheit und Lebensmittelsicherheit, Institut für Tiergesundheit I, Sachgebiet TG 1 (Tierschutz)

Concept & Realisation neue denke – Agentur für Kommunikationsgestaltung, Munich [email protected]; Hirschfeld Design, Munich [email protected]; Translation & Proofreading: Veronica Stivala, [email protected]

Publisher International Society of Livestock Husbandry

Office Veterinärwissenschaftliches Department Lehrstuhl für Tierschutz, Verhaltenskunde, Tierhygiene und Tierhaltung Tierärztliche Fakultät Ludwig-Maximilians-Universität München Veterinärstr. 13/Gebäude R D-80539 Munich

Phone +49 (0) 89 2180 78300 Fax +49 (0) 89 2180 78333

© International Society of Livestock Husbandry (IGN), Munich, Germany

All rights reserved 3 Studer (fair-fish.net); 2 Arechavala-Lopez (FishEthoGroup.net) +

Reprint—also in extracts—only with 1 permission of the publisher

Website: www.ign-nutztierhaltung.ch Cover photos: ©