B. Suffering: Stress, Distress and Pain in Fish

C. Humane Concerns in Aquaculture

• 1) Humane Slaughter
• 2) Husbandry Practices
• 3) Predator Control

D. Conclusions: Remember Charlie the Tuna

E. Reference


A. Introduction: The Problem of Fish Welfare

The first stumbling block faced when discussing the impact of fish farming on animal welfare is the fact that the overwhelming number of animals impacted  by this industry are the millions of fish held in fish farms.  The emphasis of animal welfare organizations has often been to pick a favourite, photogenic species such as the killer whale and focus on that species; of the dozens of publications in the lay press to do with the impacts of aquaculture in British Columbia, not one has focussed on the issue of the welfare of fish.  This brief will focus on one issue only, the effect of netcage salmon fish farming on the welfare of farmed fish and other animals sharing the ecosystem with farmed fish.

Welfare is defined as “the state of an animal as regards its attempts to cope with its environment” (Broome, 1986).  Welfare is not binary; it exists on a gradient from optimal to poor.  Appreciation of welfare tends to focus on the presence or absence of stress, distress, pain and suffering.  However the welfare status of animals is difficult to assess and often is subjective depending on the observational powers and experience of the viewer.  A variety of parameters can be measured as particular components of welfare, such as serum assays of the adrenal gland production of cortisol during stressed state.  The  objective variables which may vary with welfare, including mortality rate, reproductive success, adrenal hormone and  catecholamine production, behavioral changes, and incidence of disease are but a few of many means we have to make inferences of welfare status in animals.  These inferences may or may not mirror the inner state of the animal.

We are hampered scientifically and ethically by an almost complete lack of the ability to objectively assess the welfare of, and particularly to appreciate the suffering of, fish.

Do Fish Suffer?


"The question is not, can they reason? nor, can they talk? but, can they suffer?"

Jeremy Bentham,
Introduction to the Principles of Morals and Legislation, 1789

The year the Utilitarian philosopher Jeremy Bentham first addressed the issue of animal suffering in his ground breaking treatise was the same year that French revolutionaries, using an interesting new invention, the guillotine, put many thousands of aristocrats to death.  Interestingly enough, the guillotine was originally heralded as a humane invention, a device that would quickly and consistently decapitate the victim, without the messy and sometimes inaccurate attentions of an axe-wielding, sometimes drunken headsman who might take a dozen blows to sever head from body.

At the time Bentham was contemplating the fate and suffering of animals, imagine the response he must have had from his moralist and humanist colleagues in late eighteenth century Europe, wracked by war, pestilence and early death.

200 years later a similar echo of disbelief sounded when colleagues learned that the Animal Welfare Foundation of Canada was preparing a brief on the suffering of fish and other animals in aquaculture.  The response was often not so much disbelief at the concept that fish could suffer, but rather, disbelief that fish could be a subject of moral concern in a world where the suffering of humans is widespread.  However, there are nations and cultures in the Western world where the capacity of fish to suffer is recognised, and where there are legislated requirements for the humane care and treatment of animals which include fish in their mandate (Sauer and Manz, 1994).

Should humans be as concerned about the issue of suffering in fish as we are about the genocide and human suffering in Africa or Central Europe?  To sound a cautionary note, twenty years ago very few people worried about the suffering of mice and rats used for research, as opposed to dogs and primates. Now mandatory pain management plans and analgesic drugs for rodents undergoing surgery in research laboratories are the rule.  By the same token, regarding having moral concern for fish and considering how little is known about their lives and the world they live in, we should be open to considering and exploring the issue of their suffering.

We are seriously hampered in our assessment of pain, stress and suffering of all animals by several factors (Moberg 1987). First and most obvious is the fact that animals cannot directly communicate their experience to us.  Therefore we tend to rely on subjective, behavioral manifestations of stress, anxiety and pain, in animals such as facial expression and postural change. Can a fish wince?  A corollary of this is that outward manifestation of an inner state such as pain, through the universal language of behaviour which links physiological and psychological/cognitive events, can be disadvantageous in terms of Natural Selection. Imagine that you are a salmon, swimming in a school when a predator swims by. If you manifest fear in the form of behavioral response, you may be the animal which the predator notices, selects and eats, and there ends your contribution to the gene pool. Strong Darwinian forces exist which select against the outward expression of state in many animals, particularly those we call prey species, and particularly the animals sometimes termed "lower animals", the reptiles, amphibians, fish and invertebrates.

When we do encounter lower animals that show the sort of mammalian responses we approve of and identify with, we enshrine them as mammal-like.  The octopus for example, is an invertebrate cousin to the snail and clam, neither of which have much appeal as objects of moral concern.  But the octopus has big eyes, like us, a big brain, like us, interesting reproductive habits, like us, the ability to learn and even problem solve, the ability to perform a limited number of "tricks", and rather quirky responses to its environment which includes chameleonic colour and texture changes. Thus the octopus and its cephalopod brethren have become a subject of moral concern and we very closely scrutinize and regulate cephalopod use in research, because these animals have some features similar to those of higher mammals. Clearly, being mammal-like helps enlist the sympathies of man, but anyone who has looked into the cold, alien eyes of a shark knows these creatures are not mammal-like.  The extent of moral concern of humans for alien species like fish has not been great, but will likely change rapidly in the next 20 years.
 

B. Suffering: Stress, Distress and Pain in Fish

By fish, we mean teleosts, the fish with bony skeletons, as opposed to sharks, skates and rays which are cartilaginous.  By stress, we mean the normal phenomenon of physiological and behavioral changes the fish suffers in response to a stressor: a chemical, physical or social/psychological stimulus or event.  This stress response according to classical stress doctrine, consists of a 3 phase response termed the General Adaptation Syndrome (GAS)(Pickering,1981).

The 3 phases of the General Adaptation Syndrome in fish are:

1. Primary response: occurs seconds to hours after the stressor, includes alarm, with accompanying neuroendocrine response, a rapid release of ACTH (adrenal corticotrophic hormone) from the pituitary causing release of catecholamines from the head kidney and nerve endings, and cortisol from intrarenal tissue in the head kidney, as well as expression of stress proteins, such as heat shock protein in the mucus of the skin.
   
   
2. Secondary response: may include behaviour such as resistance to or flight from the stressor, while stress hormones effect target tissues, causing secondary changes such as metabolic pathway induction, and blood chemical changes (eg: increased blood glucose), as well as haematologic changes.
   
   
3. Tertiary  response: occurs some time later, from hours to days after the stressor, including whole animal ef fects of stress mediated changes like changes in growth, reproduction, osmotic tolerance, and swimming performance.
   Stress responses can be adaptive or maladaptive, so-called "good stress" and "bad stress"

Adaptive stress responses, such as increase in serum cortisol, catecholamines, and glucose, increased branchial blood flow and muscular activity, increase the likelihood of survival and adaptation over the short term.

Maladaptive stress responses decease the likelihood of long term survival and include such changes as increase in ion flux, systemic acidosis, decrease in circulating lymphocytes, and longer term negative effects on reproductive capacity and growth.

Depending on the success with which the stressed fish deals with the stressor, a variety of outcomes can occur.  Performance and survival capacity can be altered in good or bad ways.  For instance growth, disease susceptibility, and reproductive success can be enhanced by mild stressors like moderate regular exercise by supplying a constant current in a fish raceway on an aquaculture farm.  On the other hand constant high current in a netcage poorly placed in a tidal flow area causes a constant requirement for energy output to swim, in turn causing excess metabolic demands and stress, and decreased performance in growth and reproduction, and perhaps increased disease susceptibility.  An observer at a net cage site with this problem might notice some behavioral signs, such as rapid opercular rates in fish striving to get more oxygen to maintain a higher metabolic rate.

Stressors of fish can include, but are not limited to, the following types of conditions.  Susceptibility to stress can be genetically variable within species and also varies according to species of fish.  Salmonids, relative to many other species, are highly stress prone, but within salmonid genera some species are more stress prone than others.

Environmental stressors include altered water chemistry parameters, pollutants (As, CI, Cn, phenolics, PCB), metals including heavy metals (Cu, Hg, Cd, Zn, Fe).  Physical stressors include husbandry related handling, crowding, confinement, transport, pursuit and capture, sea conditions such as wave action, temperature change and current.  Biological stressors include such factors as dominance hierarchies, pathogenic microbes/parasites, toxic gases from eutrophication of wastes under salmon farms, and inadequate oxygen levels due to stocking density, activity and other factors such as water temperature.

Detecting Stressed State

A variety of means exist to infer stress is present in  fish.  These vary  from  behavioral signs (not eating, increased opercular movements) to laboratory based testing methods, such as the measurement of plasma glucose, epinephrine and cortisol.  There is a lack of currently widely used, validated means of assessing the severity of stress being suffered by fish in a rapid fashion on the seacage site (Iwama and Morgan, 1995).

Pain and Suffering in Fish

Appreciation  of the suffering of fish  from  stimuli we would regard as painful in mammals is a problematic area.  Fish, it is believed, lack mammalian nociceptors for mechanical and heat type pain reception.  They also lack the spinothalamic pathway in the spinal cord which is believed to be important in the transmission of pain information to the brain in higher vertebrates.  It has been demonstrated that elasmobranch fish lack lamina 1 of the dorsal horn of the spinal column-this  layer  in mammals, birds and reptiles transmits peripheral nociceptive information to the thalamus and subthalamic  regions associated with pain perception.  However neuropeptides associated with pain sensation such as Substance P in higher vertebrates have been identified in the dorsal horn region of the spinal cords of some elasmobranch fish (Stephens, 1995).

There has been very little research on effects of pain controlling drugs in fish.  In goldfish (Carassius auratus), morphine administration causes a graded increase in the electrical shock intensity needed to evoke an agitated swim response (Janssen and Greene, 1970), which may indicate a similar response to pain and analgesics seen in man and other higher vertebrates.  There does appear to be a natural response to pain and fear in the production of endogenous opioid substances in fish, similar to that seen in higher animals (Olson et al 1978).

There has been some research on the stress/pain responses of fish to activities such as angling, however the emphasis has been on gross parameters of welfare such as death resulting from angling. Wilkie et.al. (1996) demonstrated that up to 40 percent of angled Atlantic salmon caught and released subsequently died, depending on such factors as water temperature and time in play.

Conclusions on the Assessment of Welfare In Fish

For the purposes of providing a scientific and ethical background to the following discussion we have discussed some of the relevant facts known about the ability of fish to suffer pain and distress, and the current inadequate ability of humans to assess or understand the suffering of a fundamentally alien species.  While this may seem like a spurious issue, it is of vital importance that humans gain some understanding of the ability of fish to suffer if we are to behave in an ethical fashion when we farm these species.

Recommendation 1: Suffering

Until we have a better understanding of the ability of fish to suffer, we should operate under the principle that they have the ability to suffer, that manipulations to which they respond physiologically and behaviorally in a fashion which suggests avoidance  or escape are causes of stress and potential suffering, and that we are under a moral obligation to mitigate or minimize that suffering when we use fish as agricultural animals.
 

C. Humane Concerns in The Aquaculture Industry

The following areas of husbandry and maintenance of sea cage reared salmon are currently subjects of humane concern, both by the Animal Welfare Foundation of Canada and by other groups which have examined sea cage salmon farming in the UK and elsewhere (Farm Animal Welfare Council, 1996).  We strongly suggest that guidelines be developed to address these concerns, in conjunction with industry, keeping in mind the principles outlined in the introduction.
 

1)  Humane Slaughter of Fish

There are precedents for humane concern in the way fish are slaughtered.  As an example, methods involving the cutting of neck vessels in conscious eels were found to be inhumane (Flight and Verheijen et al. 1993).

At the present time salmon are slaughtered in a variety of ways, including immersion in CO2 and by physical means such as clubbing, followed by bleeding after loss of consciousness.  It should be noted that these means are more rapid and humane than the methods used on the vast majority of fish caught in commercial fisheries and slowly asphyxiated in nets or on the decks of vessels after capture.

CO2 Immersion

Following fasting fish are moved in very high densities (up to 150 kg/cubic meter) in special, oxygen injected live holds on packer vessels, or, alternately, may be netted and slaughtered at the farm site, usually by dubbing.  Salmon slaughter begins immediately on docking the live packer vessel at a slaughter facility.  Fish are dip netted from the fish hold into a padded polyethylene bag which is lifted every 60 seconds and emptied into a stun tank.  Approximately 20 fish are transferred each time.  A 100 gallon stainless steel tank filled with chilled water at 2-4 centigrade and saturated with compressed CO2 is used.  The fish are in the stun tank for approximately 2 minutes, after which mechanical paddles lift the fish onto a bleeding table where the branchial vessels are cut.

The fish being stunned react in different ways.  The majority thrash violently for 15-30 seconds and are quiet thereafter.  A few will "tail-walk" keeping their gills out of the water, however cutaneous CO2 absorption also occurs and these fish weaken and immerse in 30-40 seconds.  After approximately one minute of immersion the fish are quiet and there is little movement other than opercular movement, by two minutes the fish lose vertical orientation and make irregular, gasping type opercular movements, approximately 10 percent show muscle tremors.

Using standard criteria for the assessment of analgesia observers tested 20 fish immediately after stunning and found all fish unresponsive to nociceptive stimuli and unconscious.   Approximately 400 fish were observed being gill-cut for exsanguination following stunning and only one showed a feeble body twitch.  Fish are then sent to a bleeding tank held at 2-4 degrees C.  Observers did not observe any movement in the bleeding tank, indicating fish remained unconscious until death by exsanguination occurred (Harvey-Clark, 1993).

It is likely that one cause for the escape behaviour and presumably, suffering, in the use of CO2 injected water is the creation of acidic conditions through the formation of carbonic acid.  The addition of a buffer solution to the stun tank could mitigate this.

Clubbing

Observers witnessed 120 3-5 kg salmon being slaughtered by clubbing.  Fish were netted from a seacage and placed into 250 gallon fiberglass tank filled with sea ice slush and seawater using hand dip-nets.  Escape attempts were violent and prolonged in some cases for 3-5 minutes.  After fish slowed their swimming velocity to become easily handled, they were removed using a net and placed on a plastic covered table with a v-trough, where they were clubbed using an aluminum cudgel.  The fish were struck once or twice smartly in the occipital region, eliciting a body tremor followed by relaxation.  Gills were immediately cut and the fish were placed in a separate container to bleed out.  Several fish recovered the ability to swim after being cut and placed in the bleeding tank, and were removed and struck on the head.

The use of clubbing, while it appears to be effective in the majority of cases, is less consistent and is dependent on operator experience and fatigue.  It can also result in damage to the head and scale loss which in some cases results in the carcass being sold with head off, a down-grade.

Recommendation 2:  Slaughter

While C02 stunning remains the most effective and humane method currently employed, it still results in a period of 30-60 seconds of consciousness and violent escape attempts by fish.  The use of instantaneous methods which mitigate this such as electrical stunning should be revisited.
 

2)  Husbandry Practices with Fish

As with other forms of agriculture, it is apparent that the success or failure of aquaculture operations hinges on the expertise of the personnel who raise and care for fish on the site on a daily basis.  It is therefore critical to emphasize the need for the encouragement of “stockmanship” -- good husbandry practices that start with informed, concerned people working with fish.  Salmon are sensitive to husbandry, and because they require a high degree of attention in regular feeding, assessment of appetite and activity, and sensitivity to environmental factors such as temperature and the presence of predators, and other factors, the inference is that good husbandry is a foregone conclusion in any efficient operation.  Nonetheless, there are areas of welfare concern in husbandry such as fasting times where industry standards will have lasting benefit to fish, and likely will result in a better bottom line for producers.

Need for Better Basic Science for Assessment of Fish Welfare

It is apparent that more research is needed in order to develop basic parameters for the non-subjective assessment of the welfare of fish, in order to establish what constitutes good husbandry.  In particular, the need exists for tools for the assessment of pain and suffering in fish.  It is also apparent that behaviour is poorly understood in salmonids.  The need for tools for assessment of social and behavioral requirements of fish is apparent, if we are ever to appreciate whether there truly is a need for environmental enhancement in quantitative  terms (e.g., water chemistry, stocking density) or qualitative parameters (e.g., social mixing, environmental enrichment).

Having made this statement, the following are areas of animal welfare concern:

i) Handling of fish:  Care taken in handling, experience of handlers, mechanical and sorting table/grid systems and materials, immunological and disease susceptibility effects, effect of scale loss, effect of crowding, intraspecific aggression.

ii) Transport:  Usually under extremely high densities (>100 kg/cubic meter), negative effects of crowding, fasting, duration of transport are welfare concerns.

iii) Environmental  enrichment:  Salmon are highly active and kinetic fish -- what is the effect of maintaining them in the constraints of a sea cage on welfare and production parameters?

iv) Predation:  There are impacts of predation on the welfare of fish on fish farms, for instance appetite loss and increased susceptibility to infectious disease after attacks by seals.

v) Adequate environmental conditions from "cradle to grave":  It is apparent that there are periods in the life cycle of salmon where a degree of environmental stress is unavoidable such as during smoltification, hence attention should be directed towards vulnerable periods in the life cycle of sea cage reared salmon when welfare is compromised, such as periods of extreme temperature change, seasonal parasitic copepod outbreaks and toxic algae blooms.

vi) Disease Control:  Disease is an omnipresent problem in intensive fish farming and has obvious negative effects on salmon.  From a fish welfare viewpoint, proactive practices which minimize the likelihood of disease, such as quarantine, farm site selection and spacing, site fallowing and immunization, should be emphasized rather than reactive practices such as mass-medication using antibiotics.
Recommendation 3:  Husbandry

Aquaculture husbandry standards incorporating principles and concepts congruent with good stockmanship should be developed in conjunction with the aquaculture industry.
 

3) Predator Control

Sea cage salmon sites are located in the public domain on the ocean.  Harbour seals, sea lions, river otters, kingfishers, great blue herons and some fish species (dogfish, sixgill sharks) will predate netcage reared salmon and fingerlings.  In 1993 in British Columbia waters seal predation was estimated to cost as much as 40 000 dollars in direct loss of fish per net cage site, primarily due to seal predation.  Indirect losses due to stress induced fasting and immunosupression leading to disease outbreaks are difficult to assess accurately but are an additional factor.  Predators are currently being controlled primarily by shooting with high powered rifles, and as many as 500 seals per year are being shot in this fashion (EVS-Hatfield Report 1996).  A number of facilities are using acoustic deterrent devices which are reputed to decrease the incidence of seal attacks, however there is a lack of published, peer reviewed scientific literature on the efficacy of these devices.  There are documented impacts of the devices on non-target species (Harbour porpoise) to some distance around fish farms (Olesiuk et.al. 1995), and concerns about impacts on other cetacean species such as orca and humpback whales.

Perimeter anti-predator nets are in use on many BC salmon farms and evidence exists that these nets are more effective in preventing losses to large predators, when properly deployed, than shooting (Pemberton and Shaugnessy, 1993).

The environmental assessment of potential salmon farm sites must take into consideration the proximity of known marine mammal populations, and particularly predator seal/sealion haulouts.  Guidelines from government regulators to exclude new farms from within a fixed distance of marine mammal haulout sites or migratory routes should be developed.

Predator Control Recommendations:

Recommendation 4

The continued use of lethal force for control of depredation should be reviewed independently in light of evidence that alternative methods such as predator nets may be more effective, and the results published and used in determining regulatory policies on predator control.

Recommendation 5

The use of acoustic deterrent devices should be independently examined in order to determine if these devices are in fact effective in the prevention of depredation.  The impacts of these devices on non-target species must be assessed prospectively and independently by recognised authorities in the area of animal behaviour and welfare if their use is to be continued.  The ethical costs of using acoustic deterrent devices in view of their documented exclusion effects on cetacean species, particularly endangered species, must be seriously considered in the light of scientific evidence.

Recommendation 6

Research to determine new methods of preventing depredation without the documented major drawbacks of shooting and ADDs must be supported by the salmon farm industry and regulators.

Recommendation 7

Site selection criteria should exclude the consideration of seacage sites within fixed distances (5 km or greater) of known marine mammal haulout or migration routes.

Recommendation 8

Regulators are urged to facilitate the convening of meetings and workshops to encourage the development of alternatives to the existing, inadequate means of preventing predation losses on seacage salmon farms.
 

D. Conclusions: Remember Charlie the Tuna

Economic realities and world market forces ensure that the aquaculture industry will continue to exist and grow in Canada and world wide.  Whether the netcage salmon component of this industry thrives in, especially with less costly South American aquaculture salmon becoming a serious contender on the world market, will depend on a number of factors beyond the scope of this report, such as the development of trade links with South American states.  The Canadian regulatory environment could become sufficiently onerous that some aquaculture corporations will consider or threaten relocation to other countries.

It is vitally important to ensure that the animal welfare issues raised in this brief are addressed.  The welfare of those species impacted by net cage salmon farming could easily become the subject of consumer based animal activism, much in the way that the dolphin bycatch issue damaged the tuna industry in the 1980s.  As a luxury food item, seacage salmon is a ripe target for consumer based, profit-oriented fund raising campaigns of large animal rights organisations such as PETA (People for the Ethical Treament of Animals).

Consensus and progress in animal welfare issues with the West Coast salmon farm industry, which is currently entrenched in a siege mindset and perceives itself as fighting for survival, will involve changes in the defensive and secretive way the industry interacts with other interest groups.  It will also require a change in the mindset of anti-aquaculture interest groups which recognises the existence and importance of aquaculture in a biosphere with shrinking wild fish populations.  Consensus can only result from sincere efforts to look at new solutions, and recognition that animal welfare problems require attention from the aquaculture industry.  Other agri-industries have recognised and embraced the need to become proactive in ensuring welfare of animals is protected, and the netcage salmon industry can learn from this.  Government can assist this process by bringing public interests and industry together to make consensus.  The success or failure of the netcage salmon aquaculture industry in Canada and related government interests will depend on the sincerity of the regulatory processes and those people in industry and government responsible.
 

E. References

1. Broome, D.M. 1986.  Indicators of poor welfare. Br.Vet.J. 142:524-526.
2. EIlis, D.W. 1996. Net Loss: The Salmon Netcage Industry in British Columbia. David Suzuki Foundation, Vancouver.
3. Farm Animal Welfare Council of the United Kingdom. 1996. Report on the Welfare of Farmed Fish. Minis try of Agriculture, Fisheries and Food, Surbiton, U.K.
4. Flight, W.G.F. and Verheijen, F.J. 1993. The ‘neck-cut’ (spinal transection): not a humane way to slaughter eel (Anguilla anguilla L.). Aquaculture and Fisheries Management 24:523-528.
5. Harvey-Clark, C.J. 1993. Report on the British Columbia Salmon Aquaculture Industry. Canadian Farm Animal Care Trust Publication.
6. Haffield Consultants Limited and EVS Environmental Consultants. April 1996. The Environmental Effects of Salmon Netcage Culture in British Columbia. Prepared for Ministry of the Environment, Lands and Parks. 215 pp.
7. Iwama, G.K. and Morgan, J.D. 1995. Simple field methods for monitoring stress and general condition of fish. Aquaculture Research 26:273-282.
8. Jansen, G.A. and Greene, N.M. 1970. Morphine metabolism and morphine tolerance in goldfish. Anesthesiology 32:231-235.
9. Moberg, G.P. 1987. Problems in defining stress and distress in animals. JAVMA 191(1O):1207-1210.
10. Olesiuk, P.F., Nichol, L.M., Sawden, P.J. and Ford, J.K.B. 1995. Effects of sounds generated by an acoustic deterrent device on the abundance and distribution of harbour porpoise in Retreat Passage, British Columbia. DFO, Pacific Biological Station, Nanaimo, B.C.
11. Olson, R.D., Kastin, A.J., Michell, G.F., Olson, G.A., Coy, D.H. and Montalbano, D.M. 1978. Effects of endorphin and enkephalin analogues on fear habituation in goldfish. Pharmacol. Biochem. Behav. 9:111-114.
12. Pemberton, D. and Shaugnessy, P.D. 1993. Interaction between seals and marine fish farms in Tasmania, and management of the problem. Aquatic Conservation: Marine and Freshwater Ecosystems 3:149-158.
13. Pickering, A.D.(ed). 1981. Stress and Fish. Academic Press, New York.
14. Sauer, N. and Manz, D. 1994. The welfare of fish. Tierarztl. Umsch. Vol. 49(10): 653-658.
15. Stephens, C.W. 1995. An amphibian model for pain research. Lab Animal 24(10): 32-36.
16. Wilkie, M.P., Davidson, K., Brobbel, M.A., Kieffer, J.D., Booth, R.K., Bielak, A.T., and Tufts, B.L. 1996. Physiology and Survival of Wild Salmon Following Angling in Warm Summer Waters. Trans. Am. Fish. Soc. 125:572-580.

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