1011
1011
1011
(Question N° EFSA-Q-2006-437)
PANEL MEMBERS
Bo Algers, Harry J. Blokhuis, Anette Bøtner, Donald M. Broom, Patrizia Costa, Mariano
Domingo, Mathias Greiner, Jörg Hartung, Frank Koenen, Christine Müller-Graf, David B.
Morton, Albert Osterhaus, Dirk U. Pfeiffer, Mohan Raj, Ronald Roberts, Moez Sanaa, Mo
Salman, J. Michael Sharp, Philippe Vannier and Martin Wierup.
SUMMARY
Following a request from the European Commission, the Panel on Animal Health and
Welfare was asked to deliver a scientific opinion on welfare aspect of the main systems of
stunning and killing of farmed Atlantic salmon (Salmo salar) in the EU.
Harvesting and processing of farmed Atlantic salmon are the same as for sea-farmed rainbow
trout (Oncorhynchus mykiss); therefore this scientific opinion and its conclusions can also be
applied to the sea farmed trout1 production.
A semi-quantitative risk assessment approach was used to rank the risks of poor welfare
associated with the different commercially applied stunning and killing methods for Atlantic
salmon. The risk assessment was also used to identify other areas of concern, as well as to
provide guidance for future research. The risk assessment was mainly based on expert
opinion, due to the limited amount of quantitative data and published peer-reviewed data on
many effects of hazards associated with killing of Atlantic salmon. Pre-slaughter stages
which have a direct impact on the welfare immediately before and during killing were
included in the risk assessment. Stunning and killing methods that are not commercially used
in Europe (e.g. carbon monoxide) were described but not included in the risk assessment. The
opportunity to develop new methods for slaughtering Atlantic salmon is considerable and
should be encouraged.
1
Scientific Opinion of the Panel on Animal Health and Welfare on a request from the European Commission on welfare
aspect of the main systems of stunning and killing of farmed Atlantic salmon. The EFSA Journal (2009) 1012, 1-77
The five stunning and killing methods assessed were: 1. Percussive stunning; 2. Electrical
stunning; 3. Carbon dioxide; 4. Live chilling; and 5. Asphyxia in ice slurry. All methods are
followed by exsanguination.
The most important hazards in the pre-slaughter phase were associated with crowding and
transfer by pumping. Excessive crowding will result in poor welfare. There is a high risk that
salmon are subjected to metabolic stress, handling stress and poor welfare (exhaustion) prior
to slaughter. Exposing salmon to air causes a major negative impact on their welfare and
should be avoided. Crowding of fish should not be performed to a level that they show signs
of distress. Indicators for distress are; colour change, escape behaviour and air gulping. Fish
should be monitored when exiting the pumping system where the presence of fresh injuries
and exhaustion are indicators of poor welfare. After pumping, there should be visual checks
for wounds and injuries and any causes of these rectified.
Two to three days of fasting are needed to reduce the metabolic rate and thus the physical
activity of the fish which may reduce distress associated with transport. Too short or too long
transport and resting period may be an issue in association with the duration of the fasting
period. Food deprivation can result in the utilisation of body fat reserves and even functional
tissue which is associated with poor welfare.
There will always be a certain risk of poor welfare involved when fish are transported live to
slaughter. In closed systems, there are a number of issues that need to be addressed to ensure
good fish welfare at slaughter such as to ensure good water quality, e.g. adequate levels of
dissolved oxygen. The effect of elevated levels of carbon dioxide, ammonium and total
organic carbon, as well as low pH on the welfare of the fish needs to be addressed. If fish are
transported under good conditions then the fish may recover from crowding and handling
during the transport and thus, transport will not affect fish welfare at slaughter.
Regarding the stunning and killing methods, percussive methods and electrical stunning were
assessed to reliably cause unconsciousness in the vast majority of salmon.
In hand held manually fed percussive systems the hazard causing the highest risk for poor
welfare is asphyxia. For automated percussive stunning the main hazard is variation of size
within the population causing a mis-stun in some fish, e.g. hitting the snout on larger fish.
Machines for stunning and killing salmon should not be used if fish may be injured, not
stunned or not rapidly killed because of their size or orientation in the machine. For
percussive machines, size adjustment of the machines should be done by skilled personnel as
it is crucial for stunning efficiency. Percussive systems should have a separate air supply or
alternatively have security valves to block the system if the pressure is reduced below a
certain threshold.
For electrical stunning the hazard is using too low electrical currents causing paralysis and
insufficient stunning. In electrical dry stunners intended for head only application, fish
entering tail first will consciously feel the electricity for a few seconds before the head
reaches the stunner and thus welfare is poor. There is some risk of poor welfare when
applying electrical stunning in water (batch) systems mainly due to mis-stuns or exhaustion
due to exposure to electrical current. For electric stunning minimum requirements of the
electric field or current should be sufficient to cause an immediate loss of consciousness, i.e.
within 1 second. Moreover, after electrical or percussive stunning fish should not recover
consciousness before being killed by exsanguination or maceration
Severance of all gill arches on both sides of the fish, or the isthmus, or piercing the heart
directly, appears to be the best methods for killing by bleeding out unconscious fish.
Exsanguination should be carried immediately after stunning and in every case before
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 2-77
Welfare aspects of stunning and killing Atlantic salmon
recovery from stunning occurs. It is essential that a sharp knife is used to cut the vessels.
Exsanguination without prior stunning is not humane and should not be used.
All stunning systems should have an appropriate backup system to enable an immediate
correction from a mis-stun.
Carbon dioxide, asphyxia on ice and asphyxia are the methods resulting in the poorest
welfare Carbon dioxide has the highest risk score because not only was it judged that
exposure to the gas causes a strong adverse reaction but it does not reliably result in
unconsciousness, thus salmon may be bled or eviscerated when conscious. Killing salmon by
asphyxia is judged to be a severe hazard.
Disease control methods used are: pharmacological (overdose of anaesthetics), electrical and
maceration all of which should be considered as part of contingency plans. In some cases,
slaughter may be performed by normal stunning and killing procedures. In order for an
overdose of anaesthetic to be a reliable and humane killing method for salmon more
knowledge is needed before being able to recommend minimum dosage and exposure times
for specific life stages, body size and water temperature. Such information would help to
ensure a minimum time to loss of consciousness and minimum induction of stress. Fish
should be stunned or be killed before using mills for maceration.
Some indicators of poor welfare may be used to assess welfare of salmon slaughter under
commercial conditions. Standard operating procedures to improve the control of the slaughter
process to prevent impaired welfare should be introduced and validated, robust and
practically feasible welfare indicators should be further developed.
Key words: fish, animal welfare, risk assessment, pre-slaughter, stunning, killing,
slaughter, disease control, Atlantic salmon, Salmo salar, rainbow trout,
Oncorhynchus mykiss
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 3-77
Welfare aspects of stunning and killing Atlantic salmon
TABLE OF CONTENTS
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 4-77
Welfare aspects of stunning and killing Atlantic salmon
Appendix E: Risk scores and magnitude of adverse welfare effects associated with stun/kill methods . 69
Appendix F: Relevant data from the questionnaire .................................................................................. 74
Glossary and abbreviations ...................................................................................................................... 76
LIST OF TABLES
Table 1. Method for assessing the state of consciousness of fish at slaughter (Kestin et al.,
2002) ............................................................................................................................... 14
Table 2. Risk and magnitude scores for welfare hazards associated with pre-slaughter
management in Atlantic salmon in Europe, in situations where the fish are directly
processed as they arrive at the abattoir............................................................................ 26
Table 3. Risk and magnitude scores for welfare hazards associated with preslaughter
management in Atlantic salmon in Europe, where the fish are in holding for an average
of 2 days (48 hours) before they are processed further. .................................................. 28
Table 4. Risk and magnitude scores for welfare hazards associated with the main
stunning/killing methods for Atlantic salmon (Salmo salar) in Europe. ........................ 31
Table 5. Risk and magnitude scores for welfare hazards associated with the main
stunning/killing methods for Atlantic salmon (Salmo salar) in Europe, cont‟d. ............ 31
Table 6. Operational indicators (to be used under field conditions) of poor welfare for critical
monitoring points. ........................................................................................................... 34
Table 7. Intensity categories for adverse effects arising from hazards associated with pre-
slaughter / slaughter operations in Atlantic salmon. ....................................................... 52
Table 8.Duration categories for adverse effects arising from hazards associated with pre-
slaughter operations in Atlantic salmon .......................................................................... 53
Table 9. Duration categories for adverse effects arising from hazards associated with
slaughter of Atlantic salmon ........................................................................................... 53
Table 10. Scoring system for total uncertainty in severity and duration of effect .................. 54
Table 12. Description of hazards related to slaughter management of Atlantic salmon (Salmo
salar) in Europe. ............................................................................................................. 58
Table 13. Parameters used in producing risk and magnitude scores for welfare hazards
associated with preslaughter management in Atlantic salmon (Salmo salar) in Europe,
where the fish are directly processed as they arrive at the abattoir. ................................ 62
Table 14. Parameters used in producing risk and magnitude scores for welfare hazards
associated with preslaughter management in Atlantic salmon (Salmo salar) in Europe,
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 5-77
Welfare aspects of stunning and killing Atlantic salmon
where the fish are in holding for an average of 3 days before they are processed further.
......................................................................................................................................... 63
Table 15. Parameters used in producing risk and magnitude scores for welfare hazards
associated with slaughter methods applied to Atlantic salmon (Salmo salar) in Europe.
......................................................................................................................................... 64
LIST OF FIGURES
Figure 1. Pathways for pre-slaughter steps from the rearing cage to the processing lines. Dots
represent events occurring on a time line from left to right. ........................................... 13
Figure 3. Risk score and magnitude of adverse welfare effect for individual hazards
associated with pre-slaughter management in salmon in Europe, where the fish are
directly processed as they arrive at the abattoir. Hazards are ranked by risk score. Black
bars show the estimated minimum and maximum values for the risk score, reflecting the
uncertainty about the probability of exposure to the hazard. .......................................... 27
Figure 4. Risk score and magnitude of adverse welfare effect for individual hazards
associated with pre-slaughter management in salmon in Europe, where the fish are held
for an average of 2 days (48 hours) before they are processed further. Hazards are ranked
by risk score. Black bars show the estimated minimum and maximum values for the risk
score, reflecting the uncertainty about the probability of exposure to the hazard........... 29
Figure 5. Sum of risk scores and magnitudes of the adverse welfare effect for main slaughter
methods applied to salmon in Europe, ranked by the sum of the risk score. .................. 33
Figure 7. Risk score and magnitude of adverse welfare effect for individual hazards
associated with the use of fully automatic percussive stunning (swim-in) systems
(method A) in Atlantic salmon, ranked by risk score. Black bars show the estimated
minimum and maximum values for the risk score, reflecting the uncertainty about the
probability of exposure to the hazard. ............................................................................. 69
Figure 8. Risk score and magnitude of adverse welfare effect for individual hazards
associated with hand fed percussive stunning systems with automatic cut (Method B) in
Atlantic salmon (Salmo salar), ranked by risk score. Black bars show the estimated
minimum and maximum values for the risk score, reflecting the uncertainty about the
probability of exposure to the hazard. ............................................................................. 69
Figure 9. Risk score and magnitude of adverse welfare effect for individual hazards
associated with hand fed percussive stunning systems with manual cut (method C) in
Atlantic salmon (Salmo salar), ranked by risk score. Black bars show the estimated
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 6-77
Welfare aspects of stunning and killing Atlantic salmon
minimum and maximum values for the risk score, reflecting the uncertainty about the
probability of exposure to the hazard. ............................................................................. 70
Figure 10. Risk score and magnitude of adverse welfare effect for individual hazards
associated with the use of live chilling combined with carbon dioxide (Method D) in
Atlantic salmon (Salmo salar), ranked by risk score. Black bars show the estimated
minimum and maximum values for the risk score, reflecting the uncertainty about the
probability of exposure to the hazard. ............................................................................. 70
Figure 11. Risk score and magnitude of adverse welfare effect for individual hazards
associated with the use of carbon dioxide only (method E) in Atlantic salmon (Salmo
salar), ranked by risk score. Black bars show the estimated minimum and maximum
values for the risk score, reflecting the uncertainty about the probability of exposure to
the hazard. ....................................................................................................................... 71
Figure 12. Risk score and magnitude of adverse welfare effect for individual hazards
associated with the use of electrical stunning - in-water (batch) systems (method F) in
Atlantic salmon (Salmo salar), ranked by risk score. Black bars show the estimated
minimum and maximum values for the risk score, reflecting the uncertainty about the
probability of exposure to the hazard. ............................................................................. 71
Figure 13. Risk score and magnitude of adverse welfare effect for individual hazards
associated with the use of electrical stunning - dry systems (method G) in Atlantic
salmon (Salmo salar), ranked by risk score. Black bars show the estimated minimum
and maximum values for the risk score, reflecting the uncertainty about the probability
of exposure to the hazard. ............................................................................................... 72
Figure 14. Risk score and magnitude of adverse welfare effect for individual hazards
associated with the use of electrical stunning – pipe line systems (method H) in Atlantic
salmon (Salmo salar), ranked by risk score. Black bars show the estimated minimum
and maximum values for the risk score, reflecting the uncertainty about the probability
of exposure to the hazard. ............................................................................................... 72
Figure 15. Risk score and magnitude of adverse welfare effect for individual hazards
associated with the use of metocaine or benzocaine (two pharmacological preparations)
(method I) in Atlantic salmon (Salmo salar), ranked by risk score. Black bars show the
estimated minimum and maximum values for the risk score, reflecting the uncertainty
about the probability of exposure to the hazard. ............................................................. 73
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 7-77
Welfare aspects of stunning and killing Atlantic salmon
BACKGROUND
Directive 93/119/EC provides conditions for the stunning and killing of farm animals. Fish
are legally part of the scope of the EU legislation but no specific provisions were ever
adopted. Following a previous request from the Commission, EFSA issued in 2004 a
scientific opinion on the welfare aspects of the principal methods for stunning and killing the
main commercial species of animals, including farmed fish. As regards farmed fish, this
opinion concluded that “Many existing commercial killing methods expose fish to substantial
suffering over a prolonged period of time.” Furthermore, „for many species, there is not a
commercially acceptable method that can kill fish humanely”. Moreover, the respective
EFSA report highlighted that different methods for stunning and killing of farmed fish must
be developed and optimised according to the species specific different needs and welfare
aspects.
“Fish are often treated as one species when it comes to regulations and legislation governing
welfare during farming or at slaughter. But, it is important to realise that a very wide
number of species of fish are farmed, with an equally wide variety of ecological adaptations
and evolutionary developments. These differences mean that different species fish reacts
differently to similar situations. For example, at a given environmental temperature, some
species like trout die relatively quickly when removed from water into air, whilst others like
eels or marine flatfish can take several hours. Similarly, in electrical stunning situations, eels
require a much larger amount of stunning current than trout or salmon to render them
unconscious. Species differences need to be taken into account when adopting particular
procedures. Processes must be developed and optimised with respect to welfare specifically
for each species. For example, it would be as unreasonable to assume that a process
developed for killing trout in freshwater would be suitable for killing tuna in the sea as it
would be to assume that a system developed for quail would be effective on ostriches.”
TERMS OF REFERENCE
In view of the above, the Commission requests EFSA to issue a scientific opinion on the
species-specific welfare aspects of the main systems of stunning and killing of farmed fish.
The opinion should assess whether the general conclusions and recommendations of the 2004
opinion apply to the species of fish specified below. Furthermore, the above mentioned
conclusions and recommendations should be updated in a species specific approach,
integrating where possible reference to welfare indicators and to new scientific developments.
Where relevant, the animal health and food safety aspects should be taken into account.
The following species should be considered: Atlantic salmon (Salmo salar), rainbow trout
(Oncorhynchus mykiss), European eel (Anguilla anguilla), gilthead seabream (Sparus
auratus), European seabass (Dicentrarchus labrax), European turbot (Scophtalmus
maximus), common carp (Cyprinus carpio), and farmed tuna (Thunnus spp.).
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 8-77
Welfare aspects of stunning and killing Atlantic salmon
ACKNOWLEDGEMENTS
The European Food Safety Authority wishes to thank the members of the Working Group for
the preparation of this opinion: Bo Algers (Chairman), Ann Lindberg (Risk Assessor), Ulf
Erikson, Anders Kiessling, and Bjørn Roth.
Mohan Raj (AHAW Panel Member) is also acknowledged for his contribution to Chapter 3.
Jeff Lines is gratefully acknowledged for providing useful technical information and
comments on the scientific report.
The AHAW Panel also would like to thank the Member States and stakeholders organisations
for the valuable comments which were evaluated by the WG Members and when considered
pertinent included in the Scientific Opinion.
The scientific coordination for this Scientific Opinion has been undertaken by the EFSA
AHAW Panel Scientific Officers Oriol Ribó, Sofie Dhollander, Ana Afonsa, Tomasz
Grudnik, and particularly Jordi Tarrés-Call, Ingfrid Slaatto Naess, and Franck Berthe.
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 9-77
Welfare aspects of stunning and killing Atlantic salmon
ASSESSMENT
The scope of this report is the welfare aspects of the killing of farmed Atlantic salmon, Salmo
salar.
The objective is to briefly describe the current salmon slaughter practices, to identify welfare
hazards and to assess welfare risks associated with those practices through a risk assessment
approach. In addition, the aim is to identify suitable welfare indicators at slaughter where they
exist.
The pre-slaughter process is only considered where evidence exists for a direct impact on
welfare at stunning and killing. Where fish welfare, immediately before and during killing or
stunning and slaughter, is affected, it has also been considered as part of the slaughter
process. Therefore, the welfare aspects of the farming phase as well as the transport of
salmon are not included in this report. Hence, the pre-slaughter period is briefly reviewed in
the Appendix A.
Emergency killing for disease control or other reasons is included in the report. However,
humane killing of individual fish, in the course of farming operations (i.e. sorting, grading, or
background morbidity) is not included.
Much of what has been written about salmon in this report is also relevant for large rainbow
trout2 production in sea water. Their physiological stress response is similar but is reported to
be expressed more vigorously in rainbow trout.
The meat quality is not part of the assessment although, references are provided in the text
that could be used and evaluated for further socio-economic studies on slaughtering methods
for salmon.
Meat quality and safety are not part of the assessment. Food safety issues are addressed by the
BIOHAZ panel of the EFSA.
In drafting this Scientific Opinion, the panel did not take into consideration any ethical,
socio-economic, human safety, cultural or religious or management issues, the emphasis has
been to look at the scientific evidence and to interpret that in the light of the terms of
reference. Nevertheless, it is acknowledged that such aspects can have an important impact
on animal welfare.
Killing and pre-slaughter treatment of salmon comprises several operations that can have a
considerable impact on the welfare of the fish. If they are routinely fasted (1-2 weeks) and
transported by well-boat using an open system (good water exchange), there are no particular
reasons to assume their welfare at stunning and killing is affected (Erikson et al., 1997;
Erikson, 2001; Farrell, 2006). Closed systems for transport (re-circulated water) may
2
For citation purposes: Scientific Opinion of the Panel on Animal Health and Welfare on a request from the European
Commission on Species-specific welfare aspects of the main systems of stunning and killing of farmed carp. The EFSA
Journal (2009) 1013, 1-77
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 10-77
Welfare aspects of stunning and killing Atlantic salmon
facilitate slaughter but may also pose other welfare problems during transport (poor water
quality issues) (Erikson, 2001).
It is clear that pre-stunning procedures (crowding and pumping) are often very stressful to the
fish meaning they will often arrive at the stunning or killing units in a more or less exhausted
state (Erikson, 2008; Mejdell et al., 2009). The major steps from farm cage to the slaughter
plant are described in Appendix A.
For optimal operation, some of the new stunning or killing units require that the fish entering
the unit are not stressed, otherwise proper operation will be difficult to achieve, and the
welfare of the animal may be compromised.
2.2. Crowding before pumping
When the fish are to be slaughtered, they are pumped, either directly from the well-boat, or
from the holding cage, typically located near the plant quayside. Where salmon are
slaughtered on site, they are brailed or pumped directly to the stunner. New well boat
technology using movable bulkheads can probably provide better fish welfare during
unloading (see Appendix A). In fish cages, batches of salmon are collected using a sweep net
to increase fish density. Today, pressure-vacuum pumps have largely replaced lift nets for
this operation and salmon are sucked into a funnel-shaped entry to the hose (35-38 cm in
diameter) leading to the pump. During one shift (7 hours), it is common to process fish from
at least two cages and up to more than 150 metric tonnes can be processed per shift. For
example, with an average fish size of 4 kg, this means that approximately 5000 fish are
slaughtered every hour, or 1-2 fish every second.
Typically, fish density is often increased as the volume of the cage or other container is
gradually decreased. Fish are typically exposed to this potentially stressful incident for a few
minutes up to a few hours. If care is not exercised, the fish can be exposed to air, i.e. by
lifting the net too close to the water surface and severe crowding can occur. The skill of the
personnel is considered an essential factor in order to minimize handling stress during this
operation but personnel should also realise that good fish welfare and convenience may not
always go together. It is well-known that fish can change their skin colour as a response to a
stressor and in fact, skin colour changes have been suggested as welfare indicators in
aquaculture (Iger et al., 2001; Pavlidis et al., 2006). Often, as the salmon are subjected to
crowding in the cage and pumping, their dorsal skin colour changes from grey/black to
blue/green indicating a stress response.
Furthermore, it has been shown that white muscle pH tends to decrease as the fish density
increases towards the end of the pumping operation, indicating the last batches of fish are
more stressed as they are pumped on to stunning and killing operations (unpublished field
observations). Crowding of salmon prior to live chilling and slaughter has been shown to
significantly increase cortisol, glucose, lactate and osmolarity in blood plasma (Skjervold et
al., 2001) and a loss of scales (probably also involving loss of mucus) is often seen.
Control points include: monitoring of fish behaviour (e.g. video), checking levels of
dissolved oxygen, avoiding exposing fish to air and, if possible, avoiding excessive
crowding.
2.3. Transfer of fish to the stunning unit
Salmon will respond to a current by actively swimming against it. This behaviour is an
advantage in fish can be moved voluntarily by applying a water current, but it can also
constitute a welfare issue. Pumping fish is a commonly used method to move fish by water
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 11-77
Welfare aspects of stunning and killing Atlantic salmon
current. In situations where metal pipe in the pump have been replaced by Plexiglas tubes,
counter current swimming behaviour is commonly observed (Roth. pers. com.). In theory a
large salmon would be able to hold position against a current below 0.8 m/s indefinitely, for
four hours against a current of 1-1.5 m/s and for tens of minutes against a current of >2-3 m/s
(Hinch and Bratty, 2000). In addition, it is well known that large salmon in the wild will
utilize turbulence, i.e. “riding the wave” and, thereby, are able to swim against or hold
position in even faster currents (Hinch and Bratty, 2000). Recent research suggests that the
salmon on average stay about 1 to 2 minutes in the pump system when transferred from
holding pen to stunning area (Mejdell et al., 2009). Most salmon leaving from such vacuum
pump systems after crowding are exhausted (Erikson, 2008; Mejdell et al., 2009) though
whether it is a result of mental or physical (swimming against the current) stress is not
known.
When the well-boat arrives at the processing plant, salmon are either transferred to the
processing line or to holding cages by using a pressure-vacuum pump. If the fish are to be
transferred to the processing line directly from the vessel, the vessel may stay for some hours
at the quayside before the unloading process starts early next morning. In such cases,
adequate water circulation is carried out using the vessel‟s circulation pumps.
Since the holding cages also are used in a production planning context, fish can be kept there
for a few hours up to a few days before they are processed. The fish are not fed during this
period. Water quality is important at this stage of the collecting and killing procedure. During
the summer season, holding cages are often oxygenated to cope with reduced oxygen
solubility and increased fish oxygen demand as the water temperature increases. In sheltered
areas, the water temperature can rise to 20 C. Oxygenation in tank environment results in
accumulation of ammonia and CO2 compromising welfare. To which extent it is relevant for
cage environment it is not known.
Pressure-vacuum pumps have largely replaced lift nets for transferring fish from well-boat or
holding cage to the processing line, and it has become more common to use twin pumps (in
parallel) rather than using a single pump. The assumed advantage of using twin pumps is that
salmon can be supplied to the processing line in a continuous flow of fish, but when a single
pump is used, the flow of fish is temporarily stopped during the cycling between vacuum and
pressure. White muscle pH values determined before and after pumping suggest that the use
of twin pumps located at the level of holding cage (low lifting height on the suction side) is
less stressful for fish than using a single pump, particularly if the lifting height is high (i.e. the
pump is placed just outside the plant premises) (Erikson, 2008). Typically, the fish are
pumped 100 - 150 m in hoses with a diameter of 35-38 cm. On the pressure side, the lifting
height is typically about 5-8 m.
Proper design of the transfer system (hoses, pump, strainer, chutes etc) from holding cage to
stunning unit is essential for good fish welfare as faulty constructions result in injuries such
as excessive scale loss and bleeding snouts. The extent of such injuries varies considerably
from plant to plant but few fish are severely injured or killed (Mejdell et al., 2009). Examples
of poor construction leading to injury are the presence of inner pipe flanges, sharp bends and
fish at high speed colliding with bulkheads, pipe walls etc, after the water has been drained
off. Inadequate attention to clearing pipe lines after transport is also a potential welfare
hazard. However, incidences of fish left / trapped in the pump system is likely to be low
judging from observations of dead or injured fish being flushed out of the system when work
is resumed the following morning.
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 12-77
Welfare aspects of stunning and killing Atlantic salmon
Welfare related data include fish behaviour (if fish are excited: tail flapping; if fish are
exhausted: passive lying on its side) and the presence of fresh external damages (fin, skin,
body).
Figure 1. Pathways for pre-slaughter steps from the rearing cage to the processing lines. Dots
represent events occurring on a time line from left to right.
Stunning methods are supposed to induce immediate or rapid (less than 1 second)
unconsciousness, and it is important for people involved in fish slaughtering operations to be
able to recognise whether a stunning operation has rendered a fish rapidly unconscious. Such
criteria have been published (Kestin et al., 2002).
For salmon, under practical field conditions, signs for the recognition for consciousness
include respiratory movements (operculum and jaw) and other coordinated swimming
movements (Kestin et al., 2002). Under field research conditions also VOR and response to
touch / pain may be used; and in laboratory research EEG responses including visual evoked
responses (VER) could be used.
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Welfare aspects of stunning and killing Atlantic salmon
Table 1. Method for assessing the state of consciousness of fish at slaughter (Kestin et al.,
2002)
Self initiated behaviour Response to Stimuli Clinical reflexes
Name Swimming Equilibrium Handling Pin prick 6V shock Eye roll opercula
movement
Procedure Observe Invert fish, Attempt to Prick lightly Stimulate Observe eye Observe
spontaneous observe catch by tail on lip with carefully on movement opercula for
swimming righting and enough lip with 6V when fish is rhythmic
behaviour response administer pressure to DC, observe rolled from movement
tail pinch, cause response side to side (similar to
observe pricking through the breathing in
response sensation to vertical mammals and
human, birds)
observe
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Welfare aspects of stunning and killing Atlantic salmon
response
Sequence of 1 2 3 5 6 7 4
observation
Score 1* Slow or Slow to Only slow or Slow and Slow and Partial VOR Slow or
abnormal right feeble reduced reduced or one eye irregular
swimming response response response shows VOR movement
e.g. upside after tail
down pinch(s)
Score 2* Normal Quickly Immediate Head shake Head shake Eyes roll Regular
swimming rights vigorous or escape or escape relative to the opercula
escape attempt attempt head whilst movement
attempt on attempting to
first remain
touch/pinch upright when
fish is rolled
*General comments, possible artefacts: This scoring system is too simplistic, i.e. all the reflexes are either present or absent.
Some comments regarding the presence of combinations of reflexes and their interpretation will be helpful.
Operational indicators suggested to be used under field conditions of poor welfare for critical
monitoring points are presented in Table 6.
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Welfare aspects of stunning and killing Atlantic salmon
mechanism(s) by which mixtures of ice and water or super cooled water induce unconscious
has not been elucidated but, it is well known that they do not induce immediate loss of
consciousness. The possibility that induction of unconsciousness with these methods would
not occur without causing distress or suffering cannot be ruled out (Roth et al., 2009). In the
absence of direct evidence, one has to rely on physiological stress responses (Figure 2,
courtesy Dr. Lluis Tort) and their time course to ascertain the impact of these methods on the
welfare of fish. Figure 2 indicates that changes, magnitude and time course, in cortisol levels
and metabolites in blood and various tissues occur within seconds, minutes and even hours of
exposure to a stressor, which should be considered in the evaluation of the humaneness of
these methods. In general, the stress response in fish concerns the principal messengers or
products of the activation of the hypothalamic-pituitary-inter-renal axis (HPI-axis) and the
brain-sympathetic-chromaffin cells axis (BSC-axis), as reviewed by Wendelaar Bonga
(1997).
Activation of the HPI-axis starts in neurons in the nucleus pre-opticus in the hypothalamus,
which releases CRH (corticotrophin-releasing hormone) in the vicinity of the corticotrophe
cells of the distal lobe of the pituitary. When stimulated with CRH, the corticotrophe cells
secrete ACTH (adrenocorticotrophic hormone), the principal stimulator of cortisol release
form the inter-renal cells of the head kidney, into the blood (Wendelaar Bonga, 1997). It is
known that for fish, a time frame of minutes (see Figure 2) is required for cortisol to increase,
whereas for catecholamines (Brain-sympathetic-chromaffin cell axis) their release occurs
within seconds. A rapid change in temperature would prevent an increase of cortisol in the
blood, as well as other metabolic changes in various tissues.
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Welfare aspects of stunning and killing Atlantic salmon
For human consumption, the methods used are: percussive stunning, electrical, CO2, live
chilling, ice slurry, all followed by exsanguination. Several combinations of these methods
are used.
3.2.2. Fish not for direct human consumption
Salmon that do not fit market criteria will be removed from the production line, often after
stunning and killed with the methods refer to in the previous section, but also they may be
killed by suffocation in air, and maceration. Degraded fish often includes sexually mature,
injured, diseased, low weight and other fish species that are caught in salmon production.
3.2.3. Emergency slaughter
Disease control methods used are: pharmacological, electrical, and maceration all of which
should be considered as part of contingency plans. Depending on whether it is a disease
outbreak or destruction of a population due to a production error or maturation, emergency
slaughter is often carried on site or fish are transported to a designated slaughter facility.
For fish designated for human consumption, emergency slaughter may follow the normal
pattern and fish of low quality will be rejected after stunning. Diseased fish not designated for
human consumption and not killed on site, are transported in closed well boats. At arrival the
fish are either stunned or / and thrown into empty tanks ensuring death by asphyxiation or by
overdose of pharmaceuticals before they are macerated and ensiled
In cases where the whole population is unfit for human consumption, emergency slaughter is
often carried out at the production site. The choice of methods will vary depending on the
amount of fish being killed, or whether it is next to sea-cages, or on land-based tanks for
production of fry or smolt. For small numbers of salmon that are easy to handle i.e. land-
based systems or broodstock fish, they are killed by hypoxia by reducing water flow to the
tanks, or by using an overdose of anaesthetics. The carcasses are placed into closed bins or
tanks and transported to a designated processing plant. In cases where large numbers of fish
are killed, designated boats for emergency slaughter are used. Due to the toxicity of
anaesthetics and the value of fish oil, the latest development is to use electrical stunning in
combination with maceration or asphyxiation, but killing by pharmacological methods is also
used by adding either metacain or benzocain directly to the water in tanks on board the
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transport boat before closed transport to destruction. The electrical stunning devices in these
cases include either dry stunning or stunning in seawater using 50 Hz AC.
Stunning should be carried out prior to maceration or exsanguination. Signs of consciousness
in fish should be monitored before destruction.
3.2.4. Killing of Broodstock
Brood stock (1 tonne of brood stock produces 4000 tonnes of fish) is usually killed by the
application of pharmacological methods (See relevant section) before destruction.
During the 1990s, at least in Norway, rather small CO2 stunning tanks were largely replaced
by bigger live chilling tanks where CO2 is added at lower levels (Erikson et al., 2006) within
the range of 80 – 200 mg l-1 (Erikson, 2008). Some small processing plants may still use
small CO2 tanks. Carbon dioxide is highly soluble in water and has a series of effects
including sedation on fish placed in water saturated with the gas. Under commercial slaughter
conditions, carbon dioxide is bubbled into a tank filled with seawater and the pH falls as it
becomes saturated. Typically, commercial tanks operate at pH levels of about 5.5 - 6.0
corresponding to CO2 levels of 200 - 450 mg l-1 (Erikson, 2008). Levels of 200 – 500 mg l-1
are necessary to render unconscious large Atlantic salmon (Bell, 1987; Iwama and Ackerman,
1994). Fish are pumped into the water and are left there until struggling stops after 2 – 4 min
(Robb, 2001; Wall, 2001; Erikson et al., 2006; Erikson 2008). Subsequently the fish are
removed and bled. Time to loss of consciousness in salmon stunned in CO2 (judged by loss
of VERs) is approximately 6 min (Robb et al., 2000a). There is a substantial body of
evidence to indicate that fish find immersion in a carbon dioxide saturated environment
aversive. On immersion in the CO2 saturated water, salmon show vigorous aversive
reactions, swimming very rapidly and making escape attempts (Wall, 2001; Robb et al.,
2000a; Roth et al., 2002). These aversive reactions cause injury and scale loss (Akse and
Midling, 1999; Robb et al., 2002; Roth et al., 2002). There is no evidence to show that carbon
dioxide has any analgesic or anaesthetic effect, just sedation which does not imply any
reduction in pain or fear. Since killing facilities do not usually change the water between
batches, it is likely that fish are also exposed to hypoxia and this has been proposed to be the
main aversive effect. However, similar behavioural reactions have been reported in fish
exposed to high levels of carbon dioxide in a hyperoxic environment (Bernier and Randall,
1998). Based on these observations, fish would appear to find immersion in a bath of CO2
saturated water very aversive. The high activity in the carbon dioxide stunning bath routinely
results in gill haemorrhage, loss of mucus, high metabolic activity and stress (Robb and
Kestin, pers. comm.), which may also be aversive for the fish..
Because fish become immobile before losing consciousness (Robb et al., 2000a), there is a
risk that fish could be exsanguinated or gutted whilst still being conscious. Industry codes
recommend that the fish should be left in CO2 saturated water for at least 4 to 5 min before
exsanguination (Anon, 1995), but observations indicate that fish are often removed when all
carcass movements stop after 2 to 3 min (Robb, pers. comm.). In practice, the fish are not
rendered unconscious by the process and are killed by subsequent exsanguination, (Robb,
pers. comm.). Failure to exsanguinate the fish effectively (which also routinely occurs) results
in fish being eviscerated when conscious (Robb, pers. comm.). Moreover, it has been shown
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Welfare aspects of stunning and killing Atlantic salmon
that salmon removed from the CO2 bath before all respiratory movements have been lost,
usually before the fish has lost brain responsiveness, can recover if placed in well-oxygenated
water. However if fish are left in the saturated CO2 solution for a prolonged period, it leads to
death.
In summary, exposure to high levels of carbon dioxide is potentially a killing method but in
commercial practice it is usually only a sedation method.
This method does not allow good welfare during killing and it is therefore difficult to
prescribe conditions that would reduce suffering.
3.3.1.2. Carbon monoxide (CO) killing
The principle behind the use of carbon monoxide (CO) is that CO binds to the haem-iron
proteins preventing neuroglobin, myoglobin and haemoglobin binding oxygen, and an animal
will lose consciousness and die of anoxia. Since a respiratory regulation of fish is associated
with oxygen (O2) levels and not carbon dioxide (CO2), there is uncertainty whether exposure
to CO followed by oxygen deficiency will cause a euphoric reaction, due to reaction with
neuroglobin, rather than asphyxia. This method is not yet used commercially. Preliminary
studies carried out by Slinde et al. (2008) show that Atlantic salmon exposed to seawater
saturated with CO causes no flight reaction or any reaction associated with stress or
discomfort. Within minutes of exposure the salmon start to lose equilibrium followed by
impaired swimming reaction, and its ability to respond to tactile stimuli is gradually lost.
Within 20 min of exposure the animal can be unconscious since basic reflexes such as eye
roll are lost. Although the animals do not show any aversive reactions towards CO saturated
water, there is a high risk that the animals will at the later stages during the stunning process
display shorter periods with convulsions. At this point the animals reach an irreversible stage
where death is inevitable.
3.3.2. Live chilling
When live chilling first introduced into the industry (late nineteen eighties to early nineties)
they were placed in front of the much smaller (3 m3) CO2 tanks and no gases were added to
the live chilling tank.
Typical observations were that during the day as salmon slaughter was in progress, the fish
passing through the tank gradually became more sedated. It was said that the chilling of live
salmon was an effective method to sedate the fish. In hindsight however, this does not appear
to be the case. The temperatures in the tanks are in most cases -1 to 3 C where seawater
temperatures vary between 5 -19 C. In comparatively large tanks, most of the water must be
re-circulated to maintain constant, low temperatures. Consequently, there is a gradual build-
up of waste products as large numbers of fish are passing through the tank during the day.
Metabolically produced carbon dioxide accumulates to levels of for example 6 - 100 mg l-1,
apparently sufficient for light sedation. When these apparently sedated fish were transferred
to the subsequent carbon dioxide stunning tank, they seemed to regain consciousness and
struggle intensively for 2-4 min until they became quiet. Gradually the use of carbon dioxide
tanks were abandoned by the industry and instead lower amounts of carbon dioxide, along
with oxygen gas, were added directly to the live chilling tanks. Even though salmon were
abruptly chilled from 19 C to 0.4 C in the tank, it still took 2 - 4 min before the fish were
sedated (Erikson, 2008). Moreover, Olsen et al. (2006) reported that when salmon were live
chilled at 1 C for 45-60 min without addition of carbon dioxide (water pH 8.0), the fish were
still very lively and difficult to handle during gill cutting. Taken together, this clearly shows
that the live chilling method is basically equivalent to the traditional carbon dioxide stunning
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Welfare aspects of stunning and killing Atlantic salmon
method with similar fish welfare concerns. Also, live chilling of salmon is known to produce
elevated levels of plasma cortisol, glucose, lactate and increased osmolality (Skjervold et al.,
2001).
In addition to accumulated carbon dioxide, water quality in general is gradually deteriorating
in the live chilling tanks during slaughter. From a number of observations of commercial
tanks, it is clear that the fish show much aversive behaviour as they are pumped into the
tanks. This is largely due to the elevated levels of carbon dioxide, but other factors such as
elevated levels of total organic carbon (TOC) clogging the gills may also have an effect
(Erikson et al., 2006, Erikson, 2008). For other possible hazards related to water quality in re-
circulated (closed) systems, refer to the section dealing with live fish transport using closed
systems in Annex I.
3.3.2.1. Live chilling without the effect of carbon dioxide
The aim is to simultaneously chill, sedate and kill the fish by suffocation. Chilling of fish
prior to killing by another method like exsanguination or carbon dioxide narcosis followed by
exsanguination is also practised as a pre-slaughter handling step to sedate or condition fish.
„Slow chilling‟ refers to the gradual lowering of the temperature of the water by refrigeration
(at the rate of approximately 1.5 C per hour), whilst the fish are supplied with sufficient
oxygen to maintain consciousness. The aim in this application is to chill and sedate the fish
whilst maintaining them conscious and alive.
Fish can be killed by „rapid chilling‟ by first cooling them rapidly and then depriving them of
oxygen. Fish are netted or pumped through a de-watering unit and within seconds added to a
relatively small tank or bin of chilled brine or ice/water slurry. If added to an ice / water
slurry, the water is sometimes drained off after a period, leaving the fish surrounded by ice.
The aim is that by depriving the fish of oxygen, either by draining the water or because the
quality of the melting ice / water is sufficiently low, the fish will succumb to hypoxia.
Temperate species of fish take longer to lose brain function when killed in ice than air. In
situations where the ambient temperature is low and the fish are already cold adapted, the fish
will suffer no effect from the ice slurry but will die by of anoxia.
Asphyxiation in ice does not result in immediate unconsciousness. It has been proposed that
when the differential between the ambient temperature of the fish and the ice slurry is
relatively great, thermal shock may shorten time to loss of brain function. When fish are
introduced to water at ambient temperature, they continue to swim actively, but when
introduced into an ice-slurry, responses can be variable. There is a growing body of evidence
that fish find introduction to chilled water stressful. Elevated plasma cortisol levels have been
reported (Donaldson, 1981; Kiessling, pers. com.), and over time plasma osmolarity is
disturbed (Rorvik et al., 2001 Roth et al., 2009). However, because of the progressive muscle
paralysis induced by cooling, it is difficult to use behavioural indices to determine whether
fish find rapid cooling aversive at later stages of the procedure.
Loss of brain function due to cooling can be reversed if the fish are removed from the cold
water too soon. Fish transferred from iced water immediately, after loss of Visual or Sensory
Evoked reactions, to water at normal temperatures recovered brain function and subsequently
muscular movement quickly (Robb and Kestin, 2002).
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The principle of percussive stunning is that the head is struck with an object with a force
sufficient enough to stun or kill instantaneously or the animal dies due to haemorrhaging in
the brain (Kestin et al., 2002; Robb and Kestin, 2002; Roth et al., 2007; Lambooij et al.,
unpublished). The force required to stun or kill is mainly dependent on the structure of the
object, and a flat hammer is more efficient than a round or cone headed hammer (Roth et al.,
2007). If a percussive hammer correctly hits the head, irreversible death will result (Roth et
al., 2007). Recent research by Lambooij et al. (unpublished), showed that when salmon is hit
on the head with sufficient force, the EEG is instantaneously lost. However, they also noted
that some animals showed no basic reflexes, despite having a conscious state EEG recording.
This indicates that a percussive hit can paralyse the animal until consciousness is lost due to
haemorrhaging in the brain.
Although commonly practised, there exists little information on optimum conditions for
transferring kinetic energy into a shock wave or shaking the brain. In principle, two
approaches are used: either a heavy bolt at lower velocity, or a lighter bolt hitting the head at
a high velocity. This can also be seen in relations to possible side effects from percussive
stunning such as injuries to the eyes, causing eye dislocation (proptosis), eye bursting or
rupture, or haemorrhaging (Roth et al., 2007). Other methods such as penetrating bolt may be
just as efficient, but require much more accuracy both to avoid convulsions or ineffective
stunning (Robb et al., 2000 b; Lambooij et al., 2002 c; Robb and Kestin, 2002).
3.3.3.2. Percussive stunning in relation to mass slaughter
The major advantage of a percussive or captive stun is that it usually kills or renders the fish
unconscious instantaneously. One of the major challenges with percussive stunning machines
is to get live fish into the machines and a correct hit to the skull. Restraining live fish, out of
the water will cause panic and flight reactions both affecting the welfare of the animal and the
capacity for loading the machines. In streamlined systems dealing with relative low numbers
of fish, manual feeding of live fish can work well. In these systems the fish exit from the
pump, and slides towards the percussive station where an operator feeds it into the percussive
machine before the fish slides to the next station for manual cutting of the gills. As the
salmon industry is moving towards fewer and larger slaughtering facilities different strategies
for loading the machines is required to meet capacity using limited manpower, including
automatic exsanguination. This can either be done automatically where the fish swims into
the system or semi-automatically where the fish is either stunned or sedated prior to manual
loading into the machine. For automated systems the challenge is not only that all fish must
swim against the current on entering the machine, be in the correct position and be aligned
correctly, but the stunning efficiency also depends on the distribution of size within the fish
population. A successful stun is first dependent on hitting the skull at the correct position,
and there is a risk that a large or mature salmon could be hit on the snout and small salmon
on the neck, hence failing to stun the salmon. In order to deal with this back up systems are
commonly put in place, where actively moving fish exiting the automatic systems are
manually stunned.
For manual or semi-automatic systems the operator has the opportunity to place the fish into
the different machines adjusted to two or more ranges size. Although these systems can cover
a wider size range than automatic systems, extremes of small or large fish may still be
manually stunned before exsanguination.
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Welfare aspects of stunning and killing Atlantic salmon
The use of electricity to stun animals before exsanguination is well established for a range of
farm animals. As with these other farmed species, farmed fish can be stunned by applying a
sufficient electrical potential across the brain to disrupt normal neural activity. This
depolarizes the neurons and probably, as in mammals, causes functional change followed by
the release of the neuro-inhibitor GABA which results in an extended period of
unconsciousness (Cook et al., 1995).
Electric stunning systems for fish are designed to ensure that the fish being stunned lose
consciousness immediately, are not exposed to pre-stun shocks, and are unable to recover
consciousness before death supervenes.
For Atlantic salmon, several studies have shown that if the fish are exposed to sufficient
electric fields in seawater, the animals can be stunned unconscious within one second (Robb
and Roth, 2003; Roth et al., 2003). Newer studies with electric dry stunning using coupled
100 Hz AC+DC shows that Atlantic salmon can be stunned unconscious within 0.5 s, having
an average current flow through head at 667 mA (Lamboiij et al., pers. com.). The frequency
of the alternating current electricity affects the voltage or field strength required to stun fish.
In general frequencies between 50 and 150 Hz appear to have the greatest effect (Roth et al.,
2004; Robb et al., 2002).
Although salmonids are stunned unconscious within one second, a prolonged electric
exposure is required in order to secure a sufficient stun lasting beyond one minute (Roth et
al., 2003; Robb et al., 2002). For Atlantic salmon a prolonged unconscious condition can
result in death as the animal will not regain opercular ventilation in time to prevent the
animal from undergoing severe hypoxia (Robb and Roth, 2003). This is a crucial factor
during exsanguination, where the fish can recovery. Newer studies by Lambooij et al.
(personal communication) show that Atlantic salmon exposed to 5 s of electricity can recover
for a short period of time within 3 min post-stun and during exsanguination. There is very
little knowledge on the current issue.
The most common difficulty with dry stunning is to ensure that the fish are not exposed to
pre-stun shocks caused, for example, by entering the machine tail first or because spasms of
the fish cause it to lose contact with the electrodes. With in-water stunning it is important to
ensure that the electric field in the water is homogeneous and that it is matched both to the
fish species and to the water conductivity (Lines and Kestin, 2004). In tank stunning system it
is also important to ensure that the batch sizes are small enough to ensure the fish are not
stressed as they are loaded into the tank before application of the electricity and that, if they
are to be bled, they can all be bled within an acceptable time of removal from the electric
field. With continuous flow tube systems it is important to ensure that the residence time in
the tube is long enough even for the fastest flowing fish.
A challenge with the development of electrical stunning systems for salmon is to avoid
carcass damage. Such damage may appear as bleeding in the flesh along the spinal column
due to rupture of the dorsal aorta and veins. The use of high frequency electrical current (500-
1000 Hz) appears reduce such damage (Roth et al., 2004; Robb, 2001). The use of coupled
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AC+DC current may also be of interest in this respect (Mejdell et al., 2009; Roth et al.,
2009b).
A second quality problem that may occur is the early onset of rigor which can be a problem
where salmon are to be processed before rigor. Early onset of rigor is probably related to the
electro-stimulation of the muscles during the stun and may be reduced by increasing the
electrical frequency and minimising the duration of the electrical application (Roth et al.,
2006; Roth et al., 2009b).
Where salmon unwanted for human consumption are being killed, death can be caused by
prolonged exposure to an electric current without further intervention (Robb et al., 2002).
Salmon of a very wide size range and of very variable morphologies can be humanely killed
by this method. This prolonged exposure is associated with drop in muscle pH, early onset of
rigor mortis, gaping and a softer texture (Roth et al., 2002, 2006, and 2008) however this is of
little consequence for these fish.
A novel approach to electric stunning which may result in high welfare standards without
compromising carcass quality is to apply an electric stun for a short time, resulting in only a
short duration of insensibility, and during this period, while the fish are not struggling, to
percussively stun them (Mejdell et al., 2009).
Another electrical approach which can occasionally be observed is to use voltages that are too
low to result in immediate insensibility. This may be followed by a voltage that stuns the fish
once the muscles have been exhausted (Robb and Kestin, 2002). Further consideration of this
approach is not necessary since it inflicts severe and extended periods of pain and hence poor
welfare.
3.3.5. Bleeding out / Exsanguination
Atlantic salmon are commonly exsanguinated after stunning or killing to improve carcass
quality. To achieve exsanguination, three or four gills are cut either manually or
automatically with machines to bleed for a period of 10 to 30 min (Wardle, 1997). For
manual cutting a knife is used to cut the gill arches before the knife is angled and the gill
arches are cut whilst pulling the knife out. Manual gill cutting is apparently the safest method
to exsanguinate the animals since the operator aims for the gills regardless of fish size and
species. A failure to exsanguinate the animal properly can occur because the knife is not in
the correct position, or because a blunt knife fails to cut the gill arches. Compared with
manual exsanguination, machines are far less efficient in bleeding the animal properly. Like
percussive machines, a successful cut is dependent on the size and orientation of the fish. For
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Welfare aspects of stunning and killing Atlantic salmon
automatic systems fish can enter the machines in a wrong position resulting in a mis-cut and
failing to exsanguinate the animal. The accuracy of the machines depends on fish size. Fish
outside of the expected range would therefore result in mis-cuts depending on the size
distribution of the population. Also exsanguination of mature males, due to their different
morphology, may result in a mis-cut either in the jaw or in the mouth cavity.
Aversive behaviour in gill cut salmon after live chilling with CO2 has been reported (Roth et
al., 2006) causing muscle pH to drop during exsanguination. Furthermore, they reported that
approximately 1 % of salmon showed signs of consciousness prior to evisceration, 30 min
after bleeding due to a mis-cut
More recent studies using EEG showed that after electrical stunning (100 Hz, 110 V, PDC for
5 s) approximately 20 % of Atlantic salmon regained consciousness for a short period of time
during exsanguination (Lambooij et al., unpublished).
3.3.6. Pharmacological methods
Humane killing by anaesthetics in commercial salmon farming is applied during the juvenile
freshwater stage and for brood stock and emergency slaughter where fish are not intended for
human consumption. In New Zealand and Chile, isoeugenol is used for stunning in
combination with exsanguination for food fish. This anaesthetic is prohibited for such use in
the EU. The mechanism of effect of isoeugenol in relation to stress is described by Zahl et al.
(2009b). A large selection of anaesthetic agents is being used in fish, but only metacaine
(MS-222) and benzocaine are used for euthanasia in salmon at the same level
(Havbrukstjensten, pers. com.). Fish are immersed in these agents to produce general
anaesthesia but their mode of action is not fully understood (Hara and Sata 2007; Ueta et al.,
2007). Robb and Kestin (2002) found that brain activity could be detected for more than 15
minutes in salmon after exposure to either of MS-222 or benzocaine.
Subjecting the fish to handling and confinement prior to immersion is likely to elicit a stress
response. Factors as crowding, netting, pumping low water quality, low oxygen, pH etc in
addition to concentration of anaesthetic and exposure time, fish size, life stage, water
temperature and salinity are all factors that are known to affect both induction time and the
stress response (see Zahl et al., 2009b - submitted). As a general rule induction time seems to
increase with body weight, while increased water temperature and stress seems to reduce it
(see Ross and Ross, 2008 and Zahl et al., 2009a - submitted) but time to loss of
consciousness may vary. Exhausted fish most likely have a longer induction time because of
malfunctioning gill exchange Also exhausted fish could easily be mistaken for an
unconscious fish.
The slow induction of unconsciousness may provide time for the fish to detect the agents due
to their very distinctive chemical properties. They may be sensed through taste and smell and
may also act as irritants to the skin. Furthermore, as the anaesthetic starts to take its effect,
loss of balance may also elicit a stress response. So the length of time needed to induce
anaesthesia is of importance. Finally, the mode of action of the compounds is likely to affect
the stress response. Anaesthetic agents may affect the endocrine system and themselves
induce elevations in plasma cortisol (Oyama, 1973; Oyama and Wakayama, 1988; Kiessling
et al., 2009). In a study by Zahl et al. (2009b) earlier reports of Kiessling et al. (2009) were
confirmed in that MS 222 exposure causes a much faster and quantitatively larger plasma
cortisol peak than exposure to benzocaine in salmon. On the other hand benzocaine leads to a
much longer and a bimodal plasma cortisol peak compared with MS-222, indicating that the
physiological stress response of salmon differed markedly according to the chemicals used.
Furthermore, in both human and veterinary medicine, anaesthesia is often preceded by
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administering a sedative in order to calm the patient and reduce stress caused by the
anaesthetic or the anaesthetic procedure. Such pre-anaesthesia sedation has been tested in
several fish species including salmon with good results in order to reduce stress (see Zahl et
al., 2009a; b).
3.3.7. Maceration
Maceration is some times used to dispose of degraded fish following stunning. Where only a
part of the population is to be discarded (sexually mature, PD infected, other fish species that
follows the salmon), fish are transported as usual to the processing plant. There, the fish to be
discarded either follows normal routines (stunning and bleeding) or they may not be stunned
or bled (small fish species, sexually mature). Stunned and not stunned fish are placed in tubs
without water. Most will die from asphyxia, but some may not before they are macerated.
There are few studies on maceration of live animals using mill type devices, but different
types of maceration equipment have been tested for the killing of day old chicks.
Homogenizing and meat mill type equipment has been used (Hillbrich, 1975; Hilbrich & van
Mickwitz, 1977; Jaksch & Mitterlehner, 1979) and technical recommendations have been
made.
3.4. Exposure to procedures at pre-slaughter and slaughter (Questionnaire)
An enquiry regarding stunning and killing methods of farmed fish was sent out to
organizations and competent authorities in 22 EU and EC countries. EFSA received 6
answers from 4 countries concerning the stunning and killing of salmon (Norway, United
Kingdom, Iceland and Greece, see Appendix F).
Pumping is by far the most common way of transferring the fish to the processing line.
Transportation by well boat is done differently in different countries. Iceland uses a closed
system with no chilling whereas the UK uses a mainly closed system with chilling. Norway
uses mainly open systems.
The methods of stunning vary between countries: Iceland uses mainly ice slurry without CO2
(75%) and some percussive stunning (25%). United Kingdom uses only percussive stunning.
Live chilling with CO2 is the most common method in Norway (51%). Other methods used in
Norway are exposure to CO2 (20%), and percussive stunning (14%), electric stunning (7%),
ice slurry without CO2 (6%), and combinations of methods (3%).
All killing for salmon is reported to be exsanguination
The salmon industry is subject to changes in legislation as well as in technical developments,
so these figures are likely to change over time. There are also reasons to believe that there are
some uncertainties about some of the received responses.
The risk assessment method used to assess the risk to welfare of farmed Atlantic salmon
when stunned and killed is described in Appendix B.
The risk assessment was applied to the stunning and slaughter of Atlantic salmon. Salmon are
either i) taken directly to slaughter on arrival at an abattoir or ii) kept at the abattoir for up to
two days (lairage). The hazards associated with both approaches were assessed, in relation to
their effect on stunning and killing in general. The parameters used in producing risk and
magnitude scores for welfare hazards are presented in Appendix D.
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The assumption that exposure to the hazard resulted in all the fish suffering the adverse effect
held for all hazards.
Definitions of intensity of an adverse effect for hazards occurring pre- and post-stunning were
defined (Table 7).
Different categorisation for duration of the adverse effect was used for pre-slaughter and
slaughter / stunning hazards (Table 8 and Table 9).
4.1. Pre-slaughter hazards
Table 2. Risk and magnitude scores for welfare hazards associated with pre-slaughter
management in Atlantic salmon in Europe, in situations where the fish are directly
processed as they arrive at the abattoir.
Hazard ID Pre-slaughter hazards Description of adverse Risk score Magnitude
effects
post-transport status
1 Fish is in metabolic stress (e.g. after stress 6.67 67
a not-well performed closed
transport)
2 Fish is injured during transport Pain associated with the 0.50 100
injury, distress
crowding
3 Fish exposed to shallow water and gill irritation, distress, 1.00 50
air exhaustion
4 Water oxygen levels low (due to distress, escape behaviour 0.25 25
poor supervision)
5a Dry brailing abrasion, exhaustion 0.03 25
5b Wet brailing distress 0.04 8
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Welfare aspects of stunning and killing Atlantic salmon
pumping
6 Poor pipe design trauma, injuries, pain 2.50 25
7 Delay in pipe due to slow water flow stress , exhaustion 0.83 8
(crowding, low oxygen)
8 Delay in pipe due to poor system stress , exhaustion 1.67 33
logistics
9 Getting stuck in vacuum pressure stress, pain, associated 0.13 25
valve with trauma
Dry brailing
Figure 3. Risk score and magnitude of adverse welfare effect for individual hazards
associated with pre-slaughter management in salmon in Europe, where the fish are
directly processed as they arrive at the abattoir. Hazards are ranked by risk score. Black
bars show the estimated minimum and maximum values for the risk score, reflecting the
uncertainty about the probability of exposure to the hazard.
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 27-77
Welfare aspects of stunning and killing Atlantic salmon
Table 3. Risk and magnitude scores for welfare hazards associated with preslaughter
management in Atlantic salmon in Europe, where the fish are in holding for an average of
2 days (48 hours) before they are processed further.
Hazard ID Pre-slaughter hazards Description of adverse Risk score Magnitude
effects
post-transport status
crowding
12 Fish exposed to shallow water and air gill irritation, distress, 1.00 50
exhaustion
13 Water oxygen levels low (due to poor distress, escape 0.25 25
supervison) behaviour
14a Dry brailing abrasion, exhaustion 0.04 25
pumping
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 28-77
Welfare aspects of stunning and killing Atlantic salmon
Magnitude*
Delay in pipe due to poor system logistics
Risk score
Fish exposed to shallow water and air
Wet brailing
Figure 4. Risk score and magnitude of adverse welfare effect for individual hazards
associated with pre-slaughter management in salmon in Europe, where the fish are held
for an average of 2 days (48 hours) before they are processed further. Hazards are ranked
by risk score. Black bars show the estimated minimum and maximum values for the risk
score, reflecting the uncertainty about the probability of exposure to the hazard.
Nine methods of stunning and slaughter were assessed (details in Appendix E). Between five
and nine hazards were identified for each method. The risk and magnitude scores for the
hazards were summed by method (Table 4 and Table 5).
The risk scores range from 36.3 (for manually fed percussive stunning systems with manual
cut) to 293.4 (for live chilling in combination with carbon dioxide (CO2). For six of the
methods of stunning / slaughter evisceration was a hazard, because the event of a mis-stun
followed by a mis-cut was regarded as possible.
Live chilling in combination with CO2 (method D) had the highest risk score because all
salmon slaughtered with this method are exposed to CO2 at levels where it is regarded highly
unlikely that they reach unconsciousness before evisceration. In addition, the CO2 tank
provides an environment where the water quality will be poor for most of the fish and all of
them are subjected to a temperature shock during the live chilling process. CO2 exposure,
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 29-77
Welfare aspects of stunning and killing Atlantic salmon
exsanguination and mis-cuts were all hazards with a maximum magnitude of the adverse
effect (100). The method of using CO2 only (without live chilling) had a slightly lower total
risk score based only on the fact that there was no hazard from temperature shock – however
this method was in every other respect regarded as being associated with the same welfare
hazards as CO2 combined with live chilling.
Most other methods had risk scores in the range between 40 and 90. The method ranked in
fourth place was electrical stunning using in-water (batch) systems. All fish slaughtered by
this method are crowded in a tank, and electrically exhausted at sub-stun voltage levels of
electricity after which they are stunned at appropriate levels; however it will take a few
seconds before they become unconscious. The differences seen in risk score between the
electrical stunning systems were mostly due to different hazards pre-stunning, where the
batch system involves crowding, and the dry system involves being in air and a potential
delay in stunning due to the position of the fish on the conveyor. The pipe system has neither
of these but does have a hazard associated with poor pipe design. For all electrical stunning
methods, it is the exposure to different levels of electric current that produces significant
welfare risks as it will take more than 1 second before fish become unconscious and
consequently, they will experience electrical shocks while conscious. The hazards with the
highest magnitude scores for all three electrical stunning methods were potential mis-cuts,
with delayed unconsciousness from a slow bleed-out, or dying from asphyxia, both with high
severity and long duration. However, these hazards had low risk scores, indicating that they
are unlikely events.
The two pharmacological methods assessed (metocaine and benzocaine) were judged as
being equivalent, and so they are presented together. They had a summary risk score
comparable with electrical stunning methods and percussive stun/kill methods. Their highest
welfare hazards arise from the distress caused by exposure to pharmaceutics, as all fish
slaughtered by this method will experience this effect. Netting prior to application of the
preparations had the second largest risk score. All hazards associated with pharmacological
methods had the highest score for duration, based on adverse effects lasting between 3 and 10
minutes. Two hazards; dying from asphyxia or dying as silage, had maximum magnitude of
the adverse effect, but were both regarded as unlikely events.
The slaughter method with the lowest risk score (36.3) was seen for one of the percussive
stun/kill methods - the hand-fed system with manual cut. The highest ranked hazards with
this system were caused by fish being handled manually and being out of water prior to
stunning. The magnitude of the adverse effect for these hazards were, however, quite low (17
for both). Still there were two hazards out of five identified that had maximum magnitude of
the adverse effect – being mis-cut or being eviscerated while conscious. The probability of
exposure to a mis-stun, and subsequent hazards like being conscious at cutting and at
exsanguination, was judged as slightly higher for the hand-fed percussive stunning system
with an automatic cut compared with manual cutting.
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 30-77
Welfare aspects of stunning and killing Atlantic salmon
Table 4. Risk and magnitude scores for welfare hazards associated with the main
stunning/killing methods for Atlantic salmon (Salmo salar) in Europe.
Hazard ID Slaughter hazards Description of adverse Risk score Magnitude
effects
A percussive stunning - swim-in system, fully automatic 41.76 400
1a1 exhaustion (swimming into distress 23.75 25
the system)
1b1 severe exhaustion (swimming distress 3.00 100
into the system)
2 mis-stun pain, stress, trauma 5.00 50
3 mis-cut; if conscious pain, trauma, stress 1.00 100
4 exsanguination; if conscious pain, trauma, stress 9.00 100
5 evisceration; if conscious pain, trauma, stress 0.01 25
1
a and b takes into account that this hazard has different levels of magnitude
Table 5. Risk and magnitude scores for welfare hazards associated with the main
stunning/killing methods for Atlantic salmon (Salmo salar) in Europe, cont‟d.
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 31-77
Welfare aspects of stunning and killing Atlantic salmon
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 32-77
Welfare aspects of stunning and killing Atlantic salmon
CO2 only
Figure 5. Sum of risk scores and magnitudes of the adverse welfare effect for main
slaughter methods applied to salmon in Europe, ranked by the sum of the risk score.
Lairage at an abattoir provides an opportunity for salmon to recover from transport prior to
slaughter.
Some of the hazards associated with unloading and moving salmon at the abattoir could be
mitigated through better management.
Methods involving exposure to CO2 involve high welfare risks. The methods that are most
robust from a welfare point of view appear to be percussive stun/kill methods and some
electrical stunning methods. However, with some electrical stunning methods, there are
inherent welfare risks (affecting all fish slaughtered by the method) associated with the use of
low voltage to exhaust fish prior to stunning.
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 33-77
Welfare aspects of stunning and killing Atlantic salmon
Some indicators of poor welfare may be used to assess welfare of fish slaughter under
commercial conditions. However, welfare indicators have not been satisfactorily assessed and
validated so far. Observation of fish response was taken into account in this approach.
Table 6 provides indication on possible operational indicators for Atlantic salmon.
Table 6. Operational indicators (to be used under field conditions) of poor welfare for
critical monitoring points.
Methods Operational indicators (in field conditions) of poor welfare for critical control points
Transport at arrival to Control points include: Control at unloading.
abattoir
Indicators of poor welfare: Trauma.
Holding cage Control points include: Same as for fish rearing
Indicators of poor welfare: Tail flapping (during air exposure), Presence of fresh
external damages (fin, skin, body), Fish remaining in pump system after cessation of
pumping (fish coming out exhausted or dead when pumping is resumed).
Carbon dioxide Control points include: Behaviour at entering and leaving the tank.
Indicators of poor welfare: In water drained, the indicator is excessive tail flapping.
In swimming in systems it is ability to swim appropriately. After stunning,
recognition of consciousness.
Electrical Control points include: Monitoring of fish immediately before and after stunning.
stunning/killing: Manual back up system (manual stunning) present. Duration of exposure to air (after
Dry stunning water drained off) before stunning should be as short as possible.
Indicators of poor welfare: In water drained, the indicator is excessive tail flapping
and orientation of fish. After stunning, recognition of consciousness.
Electrical Control points include: Monitoring of fish immediately before and after stunning.
stunning/killing: Manual back up system (manual stunning) present. Duration of exposure to air (after
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 34-77
Welfare aspects of stunning and killing Atlantic salmon
In water stunning water drained off) before stunning should be as short as possible. Control of water
(batch stunning) quality before onset of electricity.
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 35-77
Welfare aspects of stunning and killing Atlantic salmon
Conclusions
1. This Scientific Opinion on stunning and killing of Atlantic salmon evaluated the
methods currently used in farmed Atlantic salmon in Europe. Methods used in other
fish species other than those described in this Opinion may also be applicable to
Atlantic salmon.
2. Some indicators of poor welfare may be used to assess welfare of fish slaughter under
commercial conditions.
3. If fish do not show the Eye roll and 'breathing' reflexes, then they can be considered
unconscious. Paralysis or exhaustion may influence these responses.
4. If a fish shows Eye roll and Breathing reflexes but no co-ordinated activity or
response to painful stimulation, it may be unconscious or just paralysed. It should
then be given the benefit of the doubt and considered conscious.
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 36-77
Welfare aspects of stunning and killing Atlantic salmon
stress and poor welfare (exhaustion) prior to slaughter. Moreover, loss of mucus and
scales, altered skin colour, and sometimes external injury, are observed as the fish are
ready to be stunned.
14. There is a high risk of poor welfare when using live chilling and CO2 or only CO2 as
method of slaughter, in particular because high concentrations of CO2 are aversive
and the fish may recover before killing.
15. Carbon dioxide (CO2) stunning does not allow good welfare during killing and it is
therefore difficult to prescribe conditions that would reduce suffering.
16. Live chilling without CO2 does not cause immediate unconsciousness and the method
appears to be aversive to fish.
17. Methods of killing fish by chilling the fish often involve exposure to increased carbon
dioxide concentrations, low oxygen concentrations and increased gill contact with
organic mater.
18. In hand held manually fed percussive systems the hazard causing the highest risk for
poor welfare is asphyxia.
19. For automated percussive stunning the main hazards is variation of size within the
population causing a mis-stun in some fish either hitting the snout on the outermost
size ranges.
20. For electrical stunning the hazard is using too low electrical currents causing paralysis
and insufficient stunning.
21. For fish entering the electrical dry stunner, intended for head only application, with
the tail first will consciously feel the electricity for a few seconds before reaching the
head.
22. There is some risk of poor welfare when applying electrical stunning in water (batch)
system mainly due to mis-stun or electrical exhaustion.
23. Severance of all gill arches on both sides of the fish, or the isthmus, or piercing the
heart directly, appears to be the best method for killing by bleeding out unconscious
fish.
24. There is a high risk of poor welfare when benzocaine and metacaine are used in
seawater for killing salmon.
25. In order for an overdose of anaesthetic to be a reliable and humane killing method for
salmon more knowledge is needed before being able to recommend minimum dosage
and exposure times for specific life stages, body size and water temperature. Such
information would help to ensure minimum time to loss of consciousness and
minimum induction of stress.
26. Using mills for maceration, fish should be previously stunned, and fish should then be
instantaneously killed.
Recommendations
1. Standard operating procedures to improve the control of the slaughter process to
prevent impaired welfare should be introduced and relevant practical welfare
indicators developed.
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 37-77
Welfare aspects of stunning and killing Atlantic salmon
2. Since the welfare of all farmed fish species studied has been found to be poor when
they are killed by being left in air (asphyxia) or when they are exposed to carbon
dioxide in water, these methods should generally not be used for any species as
alternative methods are available.
3. A surveillance (monitoring) programme should be initiated so that data is available in
the future for an improved risk assessment and for determining improvements over
time and also for benchmarking for those involved in the slaughter of fish.
4. The opportunity to develop new methods for slaughtering salmon is considerable and
should be encouraged.
5. Valid, robust and practically feasible indicators to evaluate the welfare of salmon
during slaughter procedures need to be developed
6. Persons involved in killing fish should be trained and hence skilled in handling and
welfare.
7. Taking current knowledge into account, it seems reasonable to suggest that the fasting
period should not exceed one week if the welfare of the animal is highlighted.
8. Crowding of fish should not be performed to the level that they show distress.
Indicators for distress are: colour change, escape behaviour and air gulping.
9. Fish should be monitored when exiting the pumping system where presence of fresh
injuries and excessive exhaustion are indicators.
10. After pumping, there should be visual checks for wounds and injuries.
11. No salmon should be killed by being left in air.
12. Carbon dioxide should not be used for stunning and killing salmon. Chilling of live
fish is not at present a humane method of killing fish so should not be used, either
alone or in combination with the use of carbon dioxide.
13. Machines for stunning and killing salmon should not be used if fish may be injured,
not stunned or not rapidly killed because the size or orientation in the machine.
Unless a back–up system exists for rapid re-stunning.
14. For percussive machines, size adjustment of the machines should be done by skilled
personnel as it is crucial for stunning efficiency. All percussive stunning systems
should have a back-up system.
15. The percussive systems should have a separate air supply or alternatively have
security valves blocking the system once the pressure is reduced below to a certain
threshold.
16. All stunning systems should have an appropriate backup system to correct from mis-
stun.
17. For electric stunning minimum requirements of the electric field or current should be
sufficient to stun fish to unconsciousness within 1 second.
18. Combining electrical stunning with percussive stunning or maceration, the minimum
requirements of the current duration should prevent fish from recovering prior these
events.
19. Combining electrical stunning with exsanguination, the minimum requirements for
the current duration should prevent fish recovering during bleed-out.
20. Exsanguination without prior stunning is not humane and should not be used.
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 38-77
Welfare aspects of stunning and killing Atlantic salmon
21. When exsanguination is performed after effective stunning, major vessels, for
example 3-4 gill arch vessels on at least one side of the fish or the ventral aorta,
should be cut to ensure rapid bleed out.
22. Effective cutting of the gill arches at least on one side of the fish.
23. It is essential that a sharp knife is used to cut the vessels.
24. Exsanguination should be carried immediately after stunning and in every case before
recovery from stunning occurs.
4. Studies should be carried out to study the capability of immediate killing of fish using
mills for maceration.
5. The effects of the pre-slaughter fasting period on subsequent fish welfare at slaughter
should be studied more in depth.
6. Colour change is indicative of stress, but how it can become an indicator of poor
welfare needs further research.
7. As there is no acceptable method for the use of currently available pharmaceuticals
for euthanasia, more research is needed in this area.
8. Establishing proper control points, welfare indicators and protocols require research.
9. Improvements are needed in the transfer methods for live fish.
10. Systems should be considered to avoid pumping or transfer of fish (e.g. placing
stunners at the cage) so that only dead fish is transported to the processing plant.
11. More research is required to prevent recovery during exsanguinations, with electric
stunning systems, while minimizing muscle stimulation.
12. Principles for percussive stunning should be investigated to determine optimum ways
for transferring kinetic energy into a shock wave, to concuss the brain.
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 39-77
Welfare aspects of stunning and killing Atlantic salmon
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Skjervold PO, Fjæra SO, Østby PB, Einen O (2001) Live-chilling and crowding stress before
slaughter of Atlantic salmon (Salmo salar). Aquaculture 192, 265-280.
Tang S, C.J. Brauner, A.P. Farewell (2009) Using bulk oxygen uptake to assess the welfare
of adult Atlantic salmon, Salmo salar, during the commercial live-haul transport.
Aquaculture 286, 318-323.
Ueta, K., T. Suzuki, et al. (2007). "Local anesthetics have different mechanisms and sites of
action at recombinant 5-HT3 receptors." Regional Anesthesia and Pain Medicine 32(6):
462-470.
Van de Vis, J.W., Kestin, S.C., Robb, D.F.H., Oehlenschläger, J., Lambooij, E., Münkner,
W., Kuhlmann H., Kloosterboer, R.J. Tejada, M. Huidobro, A. Otterå, H. Roth, B..
Sørensen, N.K Akse, L. Byrne H. and Nesvadba, P. 2003. Is humane slaughter of fish
possible for industry?, Aquaculture Research 34, pp. 211–220.
Van den Burg, E.H. (2002): Neuroendocrine control of temperature acclimation in teleost
fish. PhD thesis Radboud University Nijmegen.
Wall AJ (2001) Ethical considerations in the handling and slaughter of farmed fish. In:
Farmed Fish Quality (S. Kestin and P. Wariss, Eds.), pp 108-115, Blackwell Science,
Oxford
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Welfare aspects of stunning and killing Atlantic salmon
Wardle, C., 1997. Welfare of Farmed Salmon and Impact on Post Harvest Quality. In: Robb
D. (Ed.) Minutes of workshop: Welfare of Fish at Slaughter. University of Bristol, U.K.,
4th March 1997
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W. Pennel & B.A. Barton), pp.727-758. Elsevier, Amsterdam.
Wendelaar Bonga, S.E., 1997. The stress response in fish. Physiol. Rev. 77, 591-625.
Westers H (1984) Principles of Intensive Fish Culture 109 pp. Michigan Department of
Natural Resources, Lansing, MI.
Wood CM, Turner JD, Graham MS (1983) Why do fish die after exercise? J Fish Biol 22,
189-201.
Zahl, I.H., Kiessling, A, Samuelsen, O. and Hansen, T, (a) Anaesthesia of Atlantic cod
(Gadus morhua) – effect of pre-sedation, and importance of body weight, temperature and
acute stress. Accepted with revisions in Aquaculture.
Zahl, I.H., Kiessling, A.K., Samuelsen, O.B. and Olsen, R.E. (b). Anaesthesia induces stress
in Atlantic salmon (Salmo salar), Atlantic cod (Gadus morhua) and Atlantic halibut
(Hippoglossus hippoglossus). Submitted to Fish Biochem. Physiol.
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Welfare aspects of stunning and killing Atlantic salmon
As mentioned above, the fish density is increased before loading and crowding will occur at
some point, particularly towards the end of the loading operation. This can be stressful to the
fish and fish welfare issues should therefore be paid attention to. Crowding is discussed
below in connection with the use of holding cages.
An alternative harvesting procedure is just emerging in the aquaculture industry. Here, the
fish are pumped to percussion stunning machines located on a specially designed harvesting
vessel. After stunning, the fish are bled and transferred to refrigerated seawater (RSW) tanks
on board. Then, the fish are transported to the processing plant for gutting and further
processing. From a fish welfare point of view only, this slaughter method seems to be very
attractive since repeated handling, crowding, pumping of live fish is avoided. Trials have
shown that salmon slaughtered on such a vessel can exhibit high initial muscle pH and very
long pre-rigor times, showing the fish were exposed too little ante-mortem handling stress
(Midling et al. 2008). It remains to be seen to what extent this harvesting method will be
adopted by salmon industry. Since the various operations for slaughter of the fish are in
principle similar to those occurring within the confines of the land-based processing plants,
these operations are described above in connection with crowding in holding cage, transfer of
fish to processing line, and percussion stunning.
Transport to processing plant
In Norway, practically all farmed salmonids are routinely transported by well boats to the
processing plant to be slaughtered and processed. In 2008, there were 97 vessels approved by
the Norwegian Food Safety Authority for transport of live fish and many of those were well
boats used by the salmon industry. The carrying capacity of well boats ranges from about 50
(older vessels) to 2250 m3 (newer vessels).
In principle, two transport strategies could be chosen, either using an open system or a closed
system. Since most vessels are equipped with a RSW system, chilling the live fish on board is
also possible. Due to the high water exchange rates required, the use of the RSW system is in
practice associated with closed (or semi-closed) systems only.
The most modern vessels have video systems for monitoring fish behaviour in the holds.
Water quality (dissolved oxygen, pH, temperature, and sometimes carbon dioxide) is logged
throughout the entire haul. In many cases, a fish counter is used during loading to provide
information of the total biomass taken on board as well as data on fish size distribution.
In a commercial setting, the transport economy is of course dependent on the biomass being
transported. Thus, the maximum wanted biomass to transport under the given conditions
must be balanced with what is physically possible in terms of stress, mortality and reduced
fish quality. For example, at high SW temperatures during summer, the holds are often
oxygenated to be able to keep fish densities reasonably high. If SW temperatures in the sea-
cages approaches about 18-20 C, the well boat crew can be rather reluctant to actuate
transports at all since Atlantic salmon cannot endure much handling and stress under such
conditions.
Open system
Practically all transports are carried out using an open system, meaning that fresh SW is
constantly circulated at high rates through the valves as long as the vessel is en route. Based
on oxygen uptake rates, it has been concluded that Atlantic salmon quickly recover from
loading stress (Farrell 2006). Due to the high SW exchange rates, the water quality and fish
welfare is good in the holds (Erikson 1997, 2001, Farrell 2006, Tang et al. 2009). Similarly,
when Atlantic salmon smolts are transported by well boat, it has been shown that the loading
process (including crowding and vacuum-pumping from the sea-cage) is more stressful than
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Welfare aspects of stunning and killing Atlantic salmon
the actual live transport. In fact, based on data from 5 well boat transports, the plasma
cortisol, glucose and lactate values showed that the fish recovered from stress during
transport. The fish density, SW temperature and transport duration ranged from 17 - 42 kg m-
3
, 7.9 - 9.6 C, and 4 - 40 h, respectively (Iversen et al., 2005). Moreover, under normal
transport conditions it has been shown that the white muscle stress indicators (pH and high-
energy phosphates) as well as fillet quality are not affected by transport. The transports from
cage to processing plant were carried out under the following conditions (range): dissolved
oxygen 60 -120 % saturation, transport duration 1.5 - 5 h, SW temperature 6-15 C, fish
density 119-177 kg m-3 (Erikson 1997, 2001).
A survey of 150 commercial transports of salmon with 9 different well boats revealed that no
adverse effects on fish quality were reported under the following, typical conditions: oxygen
was added to the hold in 39 % of the transports, dissolved oxygen 70-120 % saturation,
duration of transport 0.3 – 8.5 h, fish density 41 – 255 kg m-3, SW temperature 3 -17 C, and
time at quay before unloading 0 -13 h (Erikson, 2001).
An 11 h well boat transport with adult salmon at a fish density of about 100 kg m-3 and SW
temperature of 11-12 C appeared to promote good fish welfare (Farrell, 2006).
During unloading, the vessel‟s circulation pumps are providing adequate SW exchange of the
holds. Pressure-vacuum pumps have largely replaced traditional lift nets for transfer of fish
from well boat to holding cage or directly to the fish processing line. Two new concepts are
being introduced in the salmon industry. Instead of lowering the water level in the hold,
normally necessary for increasing fish density before pumping, the fish are slowly and gently
forced to swim out from the hold using a moveable bulkhead. To avoid possible crowding
stress, fish behaviour is constantly video monitored as the bulkhead gradually is decreasing
the volume of the hold. The other new unloading method is based on pressurizing the hold.
Closed system
Presently, closed system (re-circulated water) transports of adult salmon are not carried out
on a regular basis in Norway. However, on occasions, fish with diseases have been
transported to processing plants using closed systems. In such cases, the valves are closed
from just after the fish are loaded and during the time the vessel passes sheltered areas where
other fish farms are located. Out on the open sea, the valves are opened, and as the vessel
starts to approach the processing plant, located in sheltered areas, the valves are shut. Smolts
are sometimes transported in closed systems from the hatchery to the sea-cages.
The issue of transporting live salmon to the processing plant in closed systems on a routinely
basis has been raised several times over the years. The incentive for doing this has been
thought to promote better disease control, that is, if the transported fish are infected by
pathogens, an open system transport can be risky since the effluent may reach other fish
farms along the way to the processing plant. Since control of disease is presently a major
issue in the salmon industry in Chile (exporter of farmed salmon to the EU) a shift to closed
well boat transport is particularly being examined there.
Since reduced water temperature results in a decrease of metabolic rates (e.g. lower oxygen
consumption and excretion of waste products such as carbon dioxide and ammonium) and
activity levels, lowering the transport water temperature (RSW) means that a larger biomass
can be transported making the transport more cost-effective. Another incentive for using
chilled transport is that this makes it possible to deliver pre-chilled, calm fish to the
processing plant (in cases where the fish are delivered directly to the processing line).
An RSW-chilled (closed) transport has been evaluated under commercial conditions. A
modern well boat with two separate holds (250 m3 each) was loaded with salmon at the sea-
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cage. The biomass was divided equally between the holds resulting in a fish density of 90
kg/m3. The SW in one of the holds had been pre-chilled to 1 C (RSW, closed system)
whereas the other hold was operating with open valves (as traditionally) at 8 C (SW
temperature that day). During the 2-3 h of loading and transport to the plant, only the closed
hold was oxygenated (no equipment for purifying the re-circulated water was used). During
transport, the fish in the two holds behaved differently. As usual in the open system, the fish
distributed themselves reasonably equally in the whole water column. In the closed system on
the other hand, the fish tended to gather quite closely together near the bottom of the hold. In
both holds, the fish exhibited typical slow, aerobic red muscle-based swimming behaviour
although the fish in the closed hold seemed to be even more torpid. The dissolved oxygen
levels in both holds varied between 70-110 % saturation. In the open system, the water
quality basically resembled clean SW. In the closed system, the carbon dioxide levels
increased steadily up to 45 mg l-1 causing a drop in the water pH of 1.3 units from pH 8.0
(start to end of transport). The alkalinity increased from 2.25 to 2.45 μmol l-1 and the salinity
was constant at 33.3 ppt. The TAN (NH4+ + NH3) increased to 2520 μg l-1, but the toxic
fraction of this, NH3, showed only a moderate increase up to 2.0 μg l-1 which is well below
the proposed safety level for fish farming (20 μg l-1). Moreover, the water gradually became
less transparent and some foaming occurred as was seen on the water surface. Reflecting
these changes, the Colour value increased from about 2 to 8 mg Pt l-1 (distilled water = 0 mg
Pt l-1) and the total organic carbon (TOC) increased from 1.4 to 4.8 mg l-1. The concentration
of Fe3+, used as indices of blood haemoglobin (re-circulated water containing live fish has
often a reddish tint), increased from 10 to 108 μg l-1. When fish were individually netted from
the hold after the transport, they hardly struggled at all. The body temperature was then
similar to that of the transport water (1 C). It is possible that the fish were lightly sedated due
to the accumulated carbon dioxide. The plasma chloride values before (sea-cage), and after
transport of fish from the open and closed systems were 149 ± 8, 141 ± 8, and 155 ± 5 mmol
l-1, respectively. This indicated a mild stress response for the chilled fish. The white muscle
pH values of fish from both groups were typical of rested fish (pH 7.3 - 7.5). No mortalities
were observed in either hold. Summarized, the study showed that calm, pre-chilled fish could
be delivered to the processing line without loss of biomass during transport. On the other
hand, the water quality in the closed hold gradually deteriorated which lead to elevated levels
of plasma chloride and altered fish behaviour (Erikson 2001). From this study alone, it was
not clear whether fish welfare was seriously compromised.
In a simulated live fish transport (a similar closed system) experiment at fish densities of 227
– 329 kg m-3 (fish size 4 – 5 kg) for 5 h at 15 C and heavy oxygen super-saturation (up to 250
%), firstly lead to sluggish behaviour and reduced gill ventilation rate. After a while, the fish
exhibited a gulping and coughing behaviour as they kept their mouths above the water
surface. Later, brief burst of activity were observed. When the experiment was terminated
after 5 h, most fish tended to stand upright quietly at the bottom of the tank scarcely with any
gill movement at all (Erikson 2001). It is well-known that high levels of dissolved oxygen
cause reduced ventilation rate, build-up of metabolically produced carbon dioxide, and
reduced blood pH (hypercapnia and acidosis) (Hobe et al. 1984). In turn, this may affect brain
activity and thus behaviour. Notably, in a parallel experiment with a dissolved oxygen level
of 80 % saturation, the fish also exhibited adverse behaviour but less extreme. This probably
showed that also other water quality parameters may contribute to the changes in behaviour.
The plasma chloride values of fish exposed to poor water quality for 5 h showed a clear stress
response at 155 – 170 mmol l-1 whereas control fish (good water quality) exhibited values in
the range of 140 – 145 mmol l-1. The white muscle pH values of 7.3 – 7.4 on the other hand,
indicated rested fish, in accordance with the fact that no excessive struggling took place
during the entire duration of the experiment (Erikson, 2001).
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Welfare aspects of stunning and killing Atlantic salmon
Basically, RSW live chilling tanks, commonly used in connection with sedation and slaughter
of salmon, resembles closed transport systems. The holding time of the fish are much shorter
though, 20 - 60 min when used in the slaughter line. For more details on how deteriorating
water quality might affect the fish, refer to the descriptions of live chilling and carbon dioxide
sedation above.
Another factor to consider is delayed mortality. This may occur if the fish are not slaughtered
shortly after transport using closed systems. On 5 occasions, adult salmon have been crowded
in the sea-cage and then transported for about 2 h in oxygenated closed containers to our
laboratory. At arrival, with elevated levels of metabolically produced carbon dioxide (low
pH) and oxygen supersaturated transport water, the fish had probably developed acidosis
(Erikson, 2001). After transfer of the fish to large holding tanks with excellent water quality,
in 3 out of 5 cases the fish recovered within a few hours after transport. However, in the other
2 cases, the fish started to die after some hours. Within a week, all fish had died. The
following pattern was observed: fish behaviour was not normal as no shoaling took place and
several fish stayed close to the bottom of the tank and swam occasionally around in a random
pattern. Even though water exchange was good, water clarity was constantly reduced
probably due to loss of mucus and then scales. After a few days, fungi were observed on the
skin. Probably, the fish did not recover from the acidosis caused by handling and transport. It
has been suggested that intracellular acidosis may play an important role for fish death under
severe conditions where a drop in blood pH is observed (Wood et al. 1983).
According to expert observations, when mucus was lost, they probably suffered from a severe
iono-regulation failure which might have been another cause of death. These observations
show that the fish may appear quite normal just after transport, but in fact they may be so
severely stressed that they will not recover and eventually die (unpublished results). Thus, in
terms of fish welfare, this is a point to take into consideration.
Transport of fish in closed systems has recently been reviewed by the Norwegian Scientific
Committee for Food Safety (2008).
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Introduction
Overall the risk assessment was constrained due to limited scientific data and consequently a
semi-quantitative assessment was carried out often based on expert opinion. Because of this
lack of data, the Panel on Animal Health and Welfare recommends that a
surveillance / monitoring programme should be initiated for all the fish species so that in the
future it may be possible to carry out a quantitative risk assessment.
In this section, the risk assessment method used to assess the risk to welfare of farmed fish at
the time of killing is described.
Risk assessment is a systematic, scientifically based process to estimate the probability of
exposure to a hazard, and the magnitude of the effects (consequences) of that exposure. A
hazard in animal welfare risk assessment may be defined as a factor with the potential to
cause a negative animal welfare effect (adverse effect). Risk is a function of both the
probability that the hazard and the consequences (characterised by the adverse effect) occur.
Three parameters were scored to assess the importance of a hazard; the intensity of the
adverse effect that the hazard causes, the duration of the adverse effect and the probability of
exposure to the hazard. The population in question is the fish killed in the EU by the selected
method of stunning and slaughter.
The probability of exposure to the hazard corresponds to the percentage of all fish exposed to
the hazard. Thus if 4% of the all the fish killed by a particular method are exposed to a hazard
there is a probability of 0.04 that any randomly selected fish within that population is
exposed. The consequence of exposure can be assessed by scoring the intensity and the
duration of the adverse effect in the individual. The risk assessment was based on two
assumptions;
1. all fish exposed to the hazard experienced the same intensity and duration of the
adverse effect.
2. in the absence of any evidence to the contrary, it is assumed that all fish exposed to
the hazard experience the adverse effect3.
Factors which adversely affect fish welfare are considered in the risk assessment. In absence
of reliable data, the volume of fish slaughtered by each method is not taken into account.
Thus the results are not weighted by the volume of fish slaughtered by each method.
The definitions of intensity and the categories for duration of the adverse effect used for the
fish species considered in this scientific opinion are in the relevant section in each Scientific
Opinion.
In the following paragraphs the risk assessment process for hazard identification and
characterization and the probability of exposure to the hazard are described as well as the way
they were scored. Finally the risk scoring process is described.
The general risk assessment is in line with the approach previously used in the EFSA welfare
reports (EFSA, 2007a; EFSA, 2007b; EFSA 2007c; EFSA, 2008a; EFSA, 2008b; EFSA,
3
if this assumption was not found to be sound for a particular hazard an additional parameter (probability that exposure
resulted in the adverse effect) was used.
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Welfare aspects of stunning and killing Atlantic salmon
2008c; EFSA, 2008d; EFSA, 2008e) with some modifications according to the risk question
posed.
Hazard identification
The objective of the hazard identification is to identify potential welfare hazards associated
with each stunning and killing method. The identification was based on a review of the
literature and field observations. The scope of the risk assessment included the period leading
up to killing (which may be the time spent in lairage for fish killed in a slaughterhouse). The
adverse effect caused by each hazard is described. In order to consistently identify hazards
associated with stunning and killing, the relationship between the time from applying a stun
method, unconsciousness and the point at which the killing method was applied are
illustrated graphically (Figure 6).Various scenarios (A to E) in which hazards may arise were
identified as follows:
„A‟ where a fish is killed in some potentially painful way (asphyxia, bleeding out) while it is
conscious i.e. before it has been made unconscious; and
„B‟ represents a fish that has been stunned and is killed or it dies after it is unconscious;
„C‟ where a fish has been stunned but it recovers consciousness and is killed in some
potentially painful way (asphyxia, bleeding out).
„D‟ represents a fish that, like A is killed in some potentially painful way (asphyxia, bleeding
out) while it is conscious but has also suffered from the aversive nature of the stunning
method; and
„E‟ represents a fish that has been stunned and is killed or it dies after it is unconscious but
has also suffered from the aversive nature of the stunning method.
The scenarios above do not take into account hazards arising from gathering animals during
pre-slaughter or killing without stunning.
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Table 7. Intensity categories for adverse effects arising from hazards associated with pre-
slaughter / slaughter operations in Atlantic salmon.
Evaluation Score In water In air
Hazard characterisation
Intensity
If a fish is unconscious, by definition there is no adverse welfare effect at that time.
Therefore, before assessing the intensity of any adverse effects, consideration must be given
as to whether the fish is conscious or not; this is a binary judgement (i.e. degrees of
un/consciousness are not assessed). There is evidence that signs associated with
consciousness and unconsciousness at the time of killing apply to all fish species as they do
for general anaesthesia (Kestin et al., 2002). If it is conscious, the appropriate score for the
degree of intensity of the adverse effect must be selected: mild, moderate or severe. If
unconsciousness is achieved or induced with no suffering, or any pain or distress is for less
than one second, then it is assumed that there was no welfare hazard. The issue of
consciousness is mainly relevant to hazards associated with the killing method. If
unconsciousness was achieved immediately (less than one second) then it is assumed that
there was no hazard associated with the proper and effective application of that method and
so this was not included in the risk assessment.
Generic guidelines for defining intensity categories for pre-slaughter hazards and slaughter
hazards are given in Table 11. The approach taken has been to define only the mild and
severe categories; the moderate is defined as being neither mild nor severe. Thus, by default
hazards which are considered to have welfare consequences which are not in the severe or
mild category fall into the moderate category. This approach was taken as scientists are
reasonably confident in recognising the extreme states of intensity but as these states are on a
continuum, allocating a distinct moderate banding is more difficult and contentious.
Appropriate descriptions for the categories of intensity will vary between species and are
given for each species in the Scientific Opinion.
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Additionally, different definitions of intensity for the same species may be required for
hazards that occur before killing, compared with at the time of killing. The descriptions of
intensity for these pre-slaughter adverse effects are given for each species in the Scientific
Opinion.
Table 8.Duration categories for adverse effects arising from hazards associated with pre-
slaughter operations in Atlantic salmon
Duration (minutes) Score
<51 1
5 – 15 2
>15 – 60 3
> 60 4
1
adverse effects with a duration of less than one second are not scored
Table 9. Duration categories for adverse effects arising from hazards associated with
slaughter of Atlantic salmon
Duration (minutes) Score
< 0.17 (<10 second) 1 1
0.17 – 1 2
>1 – 2 3
>2 4
1
adverse effects with a duration of less than one second are not scored
Finally, each hazard was assessed and ranked by magnitude and occurrence independently of
other hazards. For some hazards there may be more than one adverse effect. For example, all
fish netted will be exposed to air, but in addition they may be injured e.g. skin lesions due to
contact with the net or other fish.
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The degree of confidence in the final estimation of risk depends on the uncertainty and
variability (Vose, 2000). Uncertainty arises from incomplete knowledge and/or when results
are extrapolated from one situation to another (e.g. from experimental to field situations)
(Vose, 2000). Uncertainty can be reduced by carrying out further studies to obtain the
necessary data, however this may not always be a practical possibility. It can also be
appraised by using expert opinion or by simply making a judgment.
Variability is a statistical and biological phenomenon and is not reducible by gathering
further information. The frequency and severity of welfare hazards will inevitably vary
between farms and countries and over time, and fish will vary individually in their responses.
However, it is not always easy to separate variability from uncertainty. Uncertainty combined
with variability is generally referred to as total uncertainty (Vose, 2000).
Total uncertainty associated exposure to the hazard was captured by estimates of the
maximum and minimum estimates of the most likely value of the proportion of the
population exposed to the hazard. For the other parameters (intensity and duration of the
adverse effect) total uncertainty was scored on a scale of 1-3 (Table 10).
Table 10. Scoring system for total uncertainty in severity and duration of effect
Score Description
Risk Characterisation
The scoring process
The scoring was undertaken by the working group in plenary. The estimates were based on
current scientific knowledge, published data, field observation and experience (as
summarised in this report).
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The minimum, most likely and maximum values for P_hazard were used to generate
minimum, most likely and maximum estimates of the risk score. If only one risk score is
given it refers to the most likely. It is also assumed that hazards usually occur independently
of each other.
Calculation of magnitude of adverse effect
The magnitude of the adverse effect is the product of the scores for intensity and duration
according to the following formula:
Magnitude score = [(I_adverse_effect /3) * (D_adverse_effect / 4)] * 100
It has a maximum score of 100. The magnitude provides an indication of the impact of the
hazard on the fish which are exposed to the hazard and experience the adverse effect. Thus a
hazard that causes a prolonged and severe adverse effect but which affects only a small
proportion of the population will have a low risk score but a high magnitude of severity
score.
Worked example – mis-stun
Mis-stun may result when a concussive stunning method is used. This will give rise to an
adverse effect. It was estimated that the adverse effect had a intensity score equal to 3. The
duration (time from mis-stun to death or re-stun) was judged to last between one and two
minutes, hence a score of 3. It was estimated that the probability that the hazard occurs was
0.04 (i.e. 4% of fish suffer a mis-stun), with minimum and maximum estimates of 0.01 and
0.10, respectively. In summary:
score for the intensity of the adverse effect (I_adverse_effect) = 3
score for the duration of the adverse effect (D_adverse_effect) = 3 (between one
and two minutes)
the probability that the hazard occurs (P_hazard) = 0.04
(ranging from a minimum estimate of 0.01 to a maximum estimate of 0.10)
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6 Being handled manually Distress because of being held in air and handled
9 Mis-cut; if conscious Failure to cut any major aorta or vein due to size.
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14 Mis-cut; if conscious Failure to cut the gill arch (unsharpened knife, partial cut).
Current is too low to stun the fish in less that 1 second. The
Electrical exhaustion (low
23 animal can consciously feel the electricity for a period 30
current or voltage)
seconds. Escape behaviour, pain, distress, exhaustion
Up to 50% of fish can enter tail first and then feel electricity
30 Fish enter tail first
for about 2 to 3 seconds before the electrods reach the head
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The EFSA Journal (2009) 2012, 62-77
APPENDIX D: PARAMETERS USED IN PRODUCING RISK AND MAGNITUDE SCORES FOR WELFARE HAZARDS
Table 13. Parameters used in producing risk and magnitude scores for welfare hazards associated with preslaughter management in Atlantic salmon
(Salmo salar) in Europe, where the fish are directly processed as they arrive at the abattoir.
Haz. Pre-slaughter hazards Intensity Duration Duration Uncertainty Probability of exposure Risk score
ID (min1) (score2)
Most Min Max Most Min Max
likely likely
post-transport status
1 Fish is in metabolic stress (e.g. after a not-well performed closed 1 3 hours 4 1 0.1 0.05 0.15 6.67 3.3 10.0
transport) 3 0
2 Fish is injured during transport 3 3 hours 4 1 0.005 0.001 0.01 0.50 0.1 1.00
0
crowding
3 Fish exposed to shallow water and air 2 30 3 1 0.02 0.01 0.05 1.00 0.5 2.50
0
4 Water oxygen levels low (due to poor supervison) 1 15 3 1 0.01 0.005 0.02 0.25 0.1 0.63
5 3
5a Dry brailing 3 1 1 1 0.001 0.000 0.01 0.03 0.0 0.25
1 0
5b Wet brailing 1 1 1 1 0.005 0.002 0.01 0.04 0.0 0.08
5 2
pumping
6 Poor pipe design 3 3 1 3 0.1 0.05 0.15 2.50 1.2 3.75
5
7 Delay in pipe due to slow water flow (crowding, low oxygen) 1 4 1 3 0.1 0.05 0.15 0.83 0.4 1.25
2
8 Delay in pipe due to poor system logistics 2 10 2 3 0.05 0.03 0.07 1.67 1.0 2.33
0
9 Getting stuck in vacuum pressure valve 3 3 1 3 0.005 0.001 0.01 0.13 0.0 0.25
3
1
Unless another time unit is indicated
2
1 = <5min, 2 = 5-15min, 3 = 15-60 min, 4 = >60min
Table 14. Parameters used in producing risk and magnitude scores for welfare hazards associated with preslaughter management in Atlantic salmon
(Salmo salar) in Europe, where the fish are in holding for an average of 3 days before they are processed further.
Haz. ID Pre-slaughter hazards Intensity Duration Duration Uncertainty Probability of exposure Risk score
(min1) (score2)
Most likely Min Max Most likely Min Max
post-transport status
10 Fish is injured during transport 3 3 days 4 1 0.005 0.001 0.01 0.50 0.1 1.00
0
lairage
11 Poor water quality (pH, DO, water temp) 1 3 days 4 1 0.005 0.001 0.01 0.17 0.0 0.33
3
crowding
12 Fish exposed to shallow water and air 2 30 3 1 0.02 0.01 0.05 1.00 0.5 2.50
0
13 Water oxygen levels low (due to poor supervison) 1 15 3 1 0.01 0.005 0.02 0.25 0.1 0.63
5 3
14a Dry brailing 3 1 1 1 0.001 0.000 0.01 0.03 0.0 0.25
1 0
14b Wet brailing 1 1 1 1 0.005 0.002 0.01 0.04 0.0 0.08
5 2
pumping
15 Poor pipe design 3 3 1 3 0.1 0.05 0.15 2.50 1.2 3.75
5
16 Delay in pipe due to slow water flow (crowding, low oxygen) 1 4 1 3 0.1 0.05 0.15 0.83 0.4 1.25
2
17 Delay in pipe due to poor system logistics 2 10 2 3 0.05 0.03 0.07 1.67 1.0 2.33
0
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 63-77
Welfare aspects of stunning and killing Atlantic salmon
18 Getting stuck in vacuum pressure valve 3 3 1 3 0.005 0.001 0.01 0.13 0.0 0.25
3
Table 15. Parameters used in producing risk and magnitude scores for welfare hazards associated with slaughter methods applied to Atlantic salmon
(Salmo salar) in Europe.
Haz. Slaughter hazards Intensity Duration Duration Uncertainty Probability of exposure Risk score
ID (min1) (score2)
Most Min Max Most Min Max
likely likely
A percussive stunning - swim-in system, fully automatic
1a exhaustion (swimming into the system) 1 2 3 1 0.95 0.9 0.99 23.75 22.50 24.75
1b severe exhaustion (swimming into the system) 3 10 4 2 0.03 0.001 0.05 3.00 0.10 5.00
2 mis-stun 3 10 2 1 0.1 0.05 0.15 5.00 2.50 7.50
sec
3 mis-cut; if conscious 3 30 4 2 0.01 0.001 0.020 1.00 0.10 2.00
4 exsanguination; if conscious 3 6 4 1 0.09 0.080 0.099 9.00 8.00 9.90
5 evisceration; if conscious 3 2 sec 1 2 0.0005 0.000 0.001 0.01 0.00 0.03
1
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 64-77
Welfare aspects of stunning and killing Atlantic salmon
1
Unless another time unit is indicated
2
1 = <0.17 min (10 sec), 2 = 0.17-1 min, 3 = 1-2 min, 4 = >2min
Haz. Slaughter hazards Intensity Duration Duration Uncertainty Probability of exposure Risk score
ID (min1) (score2)
Most Min Max Most Min Max
likely likely
E carbon dioxide only
22 exposure to high levels of CO2 3 6 4 1 1 1 1 100.00 100.0 100.00
0
23 low water quality (organic material, low pH, ammonia..) 2 6 4 2 0.9 0.8 0.95 60.00 53.33 63.33
24 exsanguination (proper) (fish are regarded as being 3 6 4 1 0.999 0.998 0.999 99.90 99.80 99.95
conscious) 5
25 mis-cut 3 6 4 2 0.001 0.000 0.002 0.10 0.05 0.20
5
26 evisceration; if conscious 3 2 sec 1 2 0.0005 0.000 0.001 0.01 0.00 0.03
1
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 65-77
Welfare aspects of stunning and killing Atlantic salmon
Haz. Slaughter hazards Intensity Duration Duration Uncertainty Probability of exposure Risk score
ID (min1) (score2)
Most Min Max Most Min Max
likely likely
H electrical stunning - pipe line system
40 experiencing electricity while conscious 3 3 sec 1 2 0.4 0.05 0.6 10.00 1.25 15.0
0
41 exsanguination; if conscious 3 2 3 2 0.2 0.1 0.3 15.00 7.50 22.5
0
42 mis-cut; if conscious 3 30 4 2 0.001 0.0001 0.002 0.10 0.01 0.20
43 evisceration; if conscious 3 2 sec 1 3 0.0005 0.0001 0.001 0.01 0.00 0.03
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 66-77
Welfare aspects of stunning and killing Atlantic salmon
1
Unless another time unit is indicated
2
1 = <0.17 min (10 sec), 2 = 0.17-1 min, 3 = 1-2 min, 4 = >2min
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 67-77
Welfare aspects of stunning and killing Atlantic salmon
59 exposure to pharmaceutics 2 3 4 2 1 1 1
60 insufficient levels of anaesthetics => prolonged exposure time 1 10 4 2 0,001 0,0005 0,002
61 mis-stun (insufficient time of exposure to anaesthetics) 1 10 4 2 0,001 0,0005 0,002
62 asphyxia; if conscious 3 6 4 1 0,001 0,0005 0,002
63 silage 3 3 4 1 0,0001 0,00005 0,0002
1
1 = <0.17 min (10 sec), 2 = 0.17-1 min, 3 = 1-2 min, 4 = >2min
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 68-77
The EFSA Journal (2009) 2012, 69-77
mis-stun
mis-cut; if conscious
evisceration; if conscious
Figure 7. Risk score and magnitude of adverse welfare effect for individual hazards
associated with the use of fully automatic percussive stunning (swim-in) systems (method
A) in Atlantic salmon, ranked by risk score. Black bars show the estimated minimum and
maximum values for the risk score, reflecting the uncertainty about the probability of
exposure to the hazard.
exsanguination; if conscious
* Bar colour
denotes degree of
uncertainty
mis-cut; if conscious
where green=low,
yellow=moderate
and red=high
mis-stun
Figure 8. Risk score and magnitude of adverse welfare effect for individual hazards
associated with hand fed percussive stunning systems with automatic cut (Method B) in
Atlantic salmon (Salmo salar), ranked by risk score. Black bars show the estimated
minimum and maximum values for the risk score, reflecting the uncertainty about the
probability of exposure to the hazard.
exsanguination; if conscious
* Bar colour
denotes degree of
mis-stun uncertainty
where green=low,
yellow=moderate
mis-cut; if conscious and red=high
Figure 9. Risk score and magnitude of adverse welfare effect for individual hazards
associated with hand fed percussive stunning systems with manual cut (method C) in
Atlantic salmon (Salmo salar), ranked by risk score. Black bars show the estimated
minimum and maximum values for the risk score, reflecting the uncertainty about the
probability of exposure to the hazard.
Figure 10. Risk score and magnitude of adverse welfare effect for individual hazards
associated with the use of live chilling combined with carbon dioxide (Method D) in
Atlantic salmon (Salmo salar), ranked by risk score. Black bars show the estimated
minimum and maximum values for the risk score, reflecting the uncertainty about the
probability of exposure to the hazard.
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 70-77
Welfare aspects of stunning and killing Atlantic salmon
Figure 11. Risk score and magnitude of adverse welfare effect for individual hazards
associated with the use of carbon dioxide only (method E) in Atlantic salmon (Salmo
salar), ranked by risk score. Black bars show the estimated minimum and maximum
values for the risk score, reflecting the uncertainty about the probability of exposure to the
hazard.
electrical pre-treatment
Magnitude*
crowding prior to stunning
Risk score
exsanguination; if conscious
Figure 12. Risk score and magnitude of adverse welfare effect for individual hazards
associated with the use of electrical stunning - in-water (batch) systems (method F) in
Atlantic salmon (Salmo salar), ranked by risk score. Black bars show the estimated
minimum and maximum values for the risk score, reflecting the uncertainty about the
probability of exposure to the hazard.
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 71-77
Welfare aspects of stunning and killing Atlantic salmon
exsanguination; if conscious
Magnitude*
asphyxia (out of water)
Risk score
fish enter tail first
experiencing electricity while conscious ;
medium voltage system (50-110 V)
experiencing electricity while conscious ; low
voltage system (<50 V) * Bar colour
denotes degree of
experiencing electricity while conscious ; high
uncertainty
voltage system (>110 V) where green=low,
mis-cut; if conscious yellow=moderate
and red=high
asphyxia; if conscious
evisceration; if conscious
Figure 13. Risk score and magnitude of adverse welfare effect for individual hazards
associated with the use of electrical stunning - dry systems (method G) in Atlantic salmon
(Salmo salar), ranked by risk score. Black bars show the estimated minimum and
maximum values for the risk score, reflecting the uncertainty about the probability of
exposure to the hazard.
Figure 14. Risk score and magnitude of adverse welfare effect for individual hazards
associated with the use of electrical stunning – pipe line systems (method H) in Atlantic
salmon (Salmo salar), ranked by risk score. Black bars show the estimated minimum and
maximum values for the risk score, reflecting the uncertainty about the probability of
exposure to the hazard.
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 72-77
Welfare aspects of stunning and killing Atlantic salmon
exposure to pharmaceutics
Magnitude*
netting Risk score
Figure 15. Risk score and magnitude of adverse welfare effect for individual hazards
associated with the use of metocaine or benzocaine (two pharmacological preparations)
(method I) in Atlantic salmon (Salmo salar), ranked by risk score. Black bars show the
estimated minimum and maximum values for the risk score, reflecting the uncertainty
about the probability of exposure to the hazard.
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 73-77
Welfare aspects of stunning and killing Atlantic salmon
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 74-77
Welfare aspects of stunning and killing Atlantic salmon
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 75-77
Welfare aspects of stunning and killing Atlantic salmon
Glossary
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 76-77
Welfare aspects of stunning and killing Atlantic salmon
Abbreviations
A Ampere
ACTH Adrenocoticotrophin hormone
AHAW Animal Health and Welfare
BSC axis Brain sympathetic – chromaffin cells axis
CAs Catecolamines
D_adverse effect the duration of the adverse effect
EFSA European Food Safety Authority
EEG Electro-encephalogram
EC European Commission
ECG Electro-cardiogram
EU European Union
HPI axis hypothalamic Pituitary interregnal axis
mA milli-Ampere
mV milli-Volts
MS Member States
µS micro-Siemens
P_hazard L the probability that the hazard occurs
SER Somato-sensory evoked reflex
SS_adverse effect the intensity of the adverse effect
TOC Total organic carbon
V Volts
VER Visual evoked reflexes
VOR Vestibulo-ocular reflex
Stunning and Killing of farmed salmon The EFSA Journal (2009) 1012, 77-77