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The aversiveness of carbon dioxide stunning in pigs
and a comparison of the CO stunner crate vs. the
2V-restrainer
E.C. Jongman
), J.L. Barnett, P.H. Hemsworth
Animal Welfare Centre, Victorian Institute of Animal Science, Sneydes Road, PriÕate Bag 7, Werribee,
Victoria 3030, Australia
Accepted 20 October 1999
Abstract
Using aversion learning techniques, the relative aversiveness of CO to pigs in comparison to a2 shock with an electric prodder, and the aversiveness of a CO -stunner crate in comparison to the2
aversiveness of a V-belt restrainer used for electric stunning were examined. The results showed that 90% CO was considerably less aversive than an electric shock with a prodder. However,2 during exposure to 90% CO all pigs lost conscious, which may have affected their memory of the2
procedure. The pigs remained conscious after exposure to 60% CO and again showed virtually2 no aversion towards the stunner crate, while an electric shock with a prodder appeared highly aversive. The aversion to the V-restrainer belt and the CO crate were similar.q2000 Published
2
by Elsevier Science B.V. All rights reserved.
Keywords: Pigs; Stunning; Carbon dioxide; Slaughturestraint; Aversion testing
1. Introduction
Carbon dioxide stunning of pigs is widely used in Europe and America, however, there are still some concerns about the effects on animal welfare. Of particular concern
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are the pungent nature of CO gas Gregory et al., 1990 and the variation in responses2
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between pig genotypes to CO stunning Grandin, 1988 . Carbon dioxide is an unpleas-2
ant gas to inhale at high concentrations for humans because of its pungency and the
)Corresponding author. Tel.:q61-3-9742-0468; fax:q61-3-9742-0400.
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E-mail address: ellen.jongman@nre.vic.gov.au E.C. Jongman .
0168-1591r00r$ - see front matterq2000 Published by Elsevier Science B.V. All rights reserved.
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induction of breathlessness Gregory et al., 1990 . Raj and Gregory 1995 found that a majority of pigs showed a strong aversion to 90% of CO . After 24 h of fasting,2
pigs refused to enter an atmosphere of 90% CO for a food reward. Exposing pigs to2
15–20 s of a 70% mixture of CO in air produced an excitation phase with movements2
which resemble escape behaviour and this response has been considered unacceptable
ŽGrandin, 1988; Gregory et al., 1990 . However, research by Forslid 1987 and Troeger. Ž .
Ž .
and Woltersdorf 1991 based on electroencephalogram recordings indicates that the animal is unconscious before reaching this phase of behaviour. Induction of uncon-sciousness prior to the excitatory response should reduce the concern for the welfare of CO -stunned pigs, although there could still be a window of time between unconscious-2
ness and insensibility to pain.
Exposure to CO is only one aspect of the slaughtering process. In fact, a number of2
components of the slaughter process may contribute to concern for animal welfare. Aspects of this process that pigs may find unpleasant or aversive and that potentially impact on welfare include lairage systems and handling systems. Delivery to the CO2
stunner is often through a raceway at ground level, where pigs enter a well-lit crate, sometimes in small groups. This is different to most electrical stunning systems, where pigs enter a V-restrainer belt. Aversive handling systems can contribute to acute stress
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prior to slaughter as well as affecting meat quality D’Souza et al., 1998 . Therefore, it is important when studying effects of stunning methods on welfare and meat quality, to study the differences in aversiveness of the components of the slaughter process such as handling systems associated with the stunning unit.
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The objectives of this study were 1 to examine the relative aversiveness of CO to2
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pigs and 2 to compare the aversiveness of a CO stunner crate to the aversiveness of a2 V-belt restrainer used for electrical stunning.
2. Materials and methods
2.1. Animals and location
The experiments took place in an experimental abattoir. There were no other activities in the abattoir at the time of training and testing. Each experiment consisted of
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two replicates. Thirty 4-month old boars Landrace=Large White were used 15 in
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each replicate in experiment 1 and another 30 boars were used in experiment 2.
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Twenty-eight 4-month old boars of the same breeding were used 14 in each replicate in experiment 3. All animals were unfamiliar with all aspects of the abattoir. For the duration of each replicate, the pigs were housed in one large group in a large pen about 20 m away from the CO crate; the pen was adjacent to the abattoir, but not part of the2 abattoir system. The pigs were housed in this pen from the day before the experiment until the experiment was completed for that particular replicate. The walkway where ease of movement was observed and the crate itself were visually isolated from the
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group pen by a solid wall. The walkway length of 15 m was bordered by steel panels and at the end, a left and then right turn led to the CO stunner while a right and then2
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from the group for their training sessions and were returned to an adjacent pen, which was separated by a wire mesh division. The pigs were fed at 0730 h, an hour before the start of the training sessions, and at 1600 h, after the training sessions were finished.
2.2. Training procedure experiments 1 and 2
The aim of experiments 1 and 2 was to compare the aversiveness of CO with a2 known aversive stimulus, an electric prodder. In order to be able to do this pigs were first trained to walk into the empty CO stunner. After the training period, they were2
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exposed to the aversive stimulus CO or prodder or a control treatment no stimulus2
at the bottom of the CO pit. Their reluctance to enter the stunning crate after treatment2
would indicate the aversiveness of CO relative to an electric prodder.2
The pigs were trained to walk into the CO stunner crate, during the first 2 days of2
the experiment, where they were rewarded with two to three pieces of apple. However, especially during the first few sessions, most pigs showed very little interest in the reward due to apparent wariness of the novel environment. If the pig was reluctant to move through the walkway, it was encouraged with increasing force by the handler. The crate was lowered into the empty CO2 pit and remained stationary for 10 s at the bottom, after which it would ascend. To ensure that all pigs were trained to a similar level of learning to enter the stunner crate, the pigs were considered trained when they walked into the CO crate while achieving the following criteria three times during the2
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last four sessions: a time limit of 26 s with a maximum of one or two handling bouts a
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push or a slap by the handler andror one or two evasions by the pig baulks and turns with a maximum of three handling bouts andror evasions. Although these criteria seem somewhat arbitrary, a pilot study indicated that pigs moved readily into the stunner crate when they where moved within these criteria. There was a maximum of 15 training sessions per day, and once a pig was considered trained no further training occurred until the next day. The same training procedure was repeated the next day to enforce the learned behaviour. Some pigs did not achieve the training criteria in 2 days, and these pigs were excluded from the study.
2.2.1. Experiment 1
After the training period, pigs were assigned to three treatments, balanced for ease of training. The aim of this experiment was to compare the aversiveness of CO and an2
electric shock. The CO2 stunner was considered a convenient way of presenting the stimuli to the pigs. Treatment was applied once on the third day, after two additional training sessions on that day to enforce the learned behaviour. Thirty minutes after treatment was applied, the pigs were induced to enter the stunner crate during testing
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sessions in the same order as when treatment was applied until they again achieved the
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previous training criteria 26 s with a maximum of three handling bouts andror
.
On the day of treatment, pigs assigned to the CO2 treatment were treated first,
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because of the time required to fill the CO2 pit 30 min . Pigs within each treatment were taken from the group pen at random and the control and prodder treatments were applied in a random order. Pigs were tested in the same order during the testing sessions after treatment as during treatment imposition.
The treatments were as follows.
Ž .1 Control: Pigs were walked individually to the entrance of the abattoir holding yard and the time and ease of movement were measured from this location to the CO2 stunner crate. After the pig entered the crate, it descended to the bottom of the CO pit,2 remained stationary for 10 s and then ascended. This procedure was identical to the training period, except pigs were not rewarded with pieces of apple.
Ž .2 Prodder: As for treatment 1, but during the stationary period at the bottom of the
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pit, the pigs were remotely given two brief electric shocks -1 s with a commercial cattle prodder. The electric prodder was used as a known aversive stimulus.
Ž .3 CO : As for the control but without a stationary period, with the pit filled with2
CO providing a concentration of 90% CO at the bottom of the pit. The concentration2 2
at the top where the pig entered the crate was close to zero. The concentration of CO2
that the pig was exposed to increased during descent into the pit, with the concentration reaching 60% halfway down the pit, and 90% at the bottom. The descent took about 15 s, and immediately after reaching the bottom, the crate ascended.
2.2.2. Experiment 2
During exposure to 90% CO in experiment 1, pigs became unconscious. There was2 some concern that their memory may have been affected, which would make the subsequent measurement of the aversiveness of the experience unreliable. Thus, experi-ment 1 was repeated with a shorter exposure to a lower concentration of CO . Again,2
pigs assigned to the CO treatment were treated first, because of the time required to fill2
the CO pit. The treatments were the same as in experiment 1, except for the following2
differences. In the control treatment, the crate descended halfway down the CO2 pit, remained stationary for 10 s and then ascended. In the prodder treatment, the two brief electric shocks were given during the stationary period halfway down the pit. In the CO2
treatment, pigs were exposed to a concentration of 60% CO halfway down the pit. The2
decent halfway down the pit took about 7 s, and immediately on reaching the halfway point, the crate ascended.
2.3. Training procedure experiment 3
The aim of experiment 3 was to compare the aversiveness of the CO crate and the2 V-restrainer belt as a restraining system during stunning. In order to be able to do this, pigs were first trained to enter the stunning systems while they were stationary. During treatment, both the CO crate and the V-belt restrainer were set in motion. Pigs were2
assigned randomly to treatment before the start of the 2-day training period. Half the pigs were trained to enter the CO stunner crate, where they were held for 30 s while the2
V-restrainer while the belt was stationary and a temporary floor was in place. The training procedure and training criteria were similar to experiments 1 and 2. Pigs were rewarded in both systems with pieces of apple. The third day started with two training sessions, followed by a session when treatments were applied, in a random order, to both groups. Following removal of the temporary floor in the V-restrainer, treatment in this system consisted of individually moving each pig to the V-belt, which was then switched on until the pig reached the other end, where it left the V-restrainer. Treatment in the CO crate consisted of individually moving each pig to the crate, lowering the2 crate to the bottom of the empty CO pit, where it remained stationary for 10 s and than2 raising the crate. After treatment was applied once to each pig, the pigs were individu-ally moved to enter the allocated stunning unit during testing sessions until they again achieved the previous training criteria three times during the last four training sessions. Ease of movement during the testing sessions after treatment was used to measure the aversiveness of the treatment applied.
2.3.1. Experiment 3
After a 2-day training period, treatment was applied on day 3. On this day, pigs were subjected to two training sessions before treatment was applied during the third session. The treatments were as follows.
Ž .1 CO crate: Pigs were walked individually to the entrance of the abattoir holding2 yard and the time and ease of movement were measured from this location to the CO2 stunner crate. After the pig entered the crate, it descended to the bottom of the CO pit2
Žwith no CO2.and then immediately ascended.
Ž .2 V-restrainer: Pigs were walked individually to the entrance of the abattoir holding yard and the time and ease of movement were measured from this location to the V-restrainer. The V-belt was set in motion at the moment the pig entered the V-re-strainer.
The raceway leading up to the two treatments was identical, with the pigs having to turn left into the CO crate and right into the V-restrainer. It was not possible to balance2
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the location left vs. right of treatments relative to the race since the CO stunner and2
V-restrainer were permanent fixtures of the experimental abattoir. The entrance to the
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CO2 crate consisted of a step down of 10 cm between narrow doors, whereas the
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entrance to the V-restrainer consisted of a slightly sloping ramp 1.5 m long, 30 cm
.
high . The CO crate was in an enclosed area, but was well lit with fluorescent lights.2
The V-restrainer was in an open space with views through the restrainer into the abattoir. The entry characteristics to the two systems are considered as inherent components of each treatment.
2.4. Statistical analysis
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An analysis of covariance Genstat 5 was performed to analyse the effects of
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blocked on replicate. Although it is recognised that the treatments were not applied at random due to practical constraints, this was not included in the statistical analysis.
3. Results
3.1. Experiment 1
The average times to enter the CO crate on the day of treatment are presented in2
Table 1. Only pigs that met the training criteria during the training sessions on days 1 and 2 were included in the experiment. In the first replicate, 11 of 15 pigs were trained, with three pigs assigned to the control treatment, four pigs to the CO treatment and four2 pigs to the prodder treatment. In the second replicate all pigs were trained, with five pigs
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assigned to each treatment. After two training sessions on day 3, treatments control,
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90% CO or prodder were applied during the next session labelled session 0 . Because2
treatment was applied after the pigs entered the CO crate, the times during session 02
would not have been affected by treatment. While there was no treatment effect during
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session 1 P)0.05 , time to re enter was significantly greater in the prodder than the
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control treatment in sessions 2, 3, 4 and 5 P-0.05, P-0.01, P-0.001 and
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P-0.05, respectively . There were no P)0.05 differences between the CO and the2 Ž .
control treatments. Time to re enter was significantly greater in the prodder than the
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CO treatment in sessions 4, 6 and 7 P2 -0.05 .
3.2. Experiment 2
The average times to enter the CO crate on the day of treatment during experiment 22
are presented in Table 2. In the first replicate, 12 of 15 pigs were trained, with four pigs
Table 1
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Experiment 1: Average times s to re enter stunning unit on the day of treatment, with treatment applied during session 0
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Control 90% CO2 Electric prodder LSD P-0.05
Table 2
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Experiment 2: Average times s to re enter stunning unit on the day of treatment, with treatment applied during session 0
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Control 60% CO2 Electric prodder LSD P-0.05
Session 0 30.6 30.2 27.0 8.59
per treatment. In the second replicate, all 15 pigs were trained, with five pigs per
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treatment. Treatments were applied on day 3 session 0 after two training sessions. No
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differences were found between treatments in time to re enter the crate during session 1
ŽP)0.05 . However, there were significant P. Ž -0.05 differences between the control.
treatment and the electrical prodder during sessions 3 and 4. There were no significant
ŽP)0.05 differences between the CO and the control treatments during any of the. 2
sessions.
3.3. Experiment 3
There is some indication that the CO crate may be slightly more aversive than the2
V-restrainer belt when the pigs are first presented to these stunning units. The average
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times to enter both stunning units CO crate and V-restrainer belt for the first time on2
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the first training day were 38.6 and 22.0 s, respectively P-0.05 . The difference between the two units disappeared after training.
The average times to enter the stunning units on the day of treatment are presented in Table 3. In the first replicate 12 of 14 pigs were trained, with six pigs per treatment. In the second replicate, all 14 pigs were trained with seven pigs per treatment. Treatment on day 3 was applied during session 0. Descent in the crate or transport through the
Table 3
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Experiment 3: Average times s to re enter the stunning unit on the day of treatment, with treatment applied during session 0
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CO crate2 V-restrainer LSD P-0.05
Session 0 17.9 19.3 3.16
Session 1 18.4 17.4 2.51
Session 2 18.4 16.4 2.31
Session 3 18.4 16.8 2.25
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V-belt restrainer in operation did not significantly change the time to re enter either
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stunning unit P)0.05 .
4. Discussion
The results of experiment 1 suggest that a single exposure to 90% CO was, at the2 most, only slightly more aversive than the control treatment and considerably less aversive than an electric shock with a prodder. However, during exposure to 90% CO2
all pigs lost consciousness. If unconsciousness was associated with anoxia to the brain, it may have affected the pigs’ memory of the procedure. To overcome this problem, in experiment 2, pigs were only lowered halfway down the CO2 pit were the CO2
concentration was 60%. These pigs hyperventilated mildly, but did not lose conscious-ness, thus memory should not have been affected. The results of experiment 2 were very similar to the first experiment, with CO being only mildly aversive and considerably2
less aversive than an electric prodder. The findings of this study are contrary to the
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findings of a study by Raj and Gregory 1995 . In that study, pigs avoided a food reward in 90% CO , and to a lesser extent 60% CO , even after a 24 h fasting period and the2 2 authors concluded that CO was very aversive to pigs. However, no negative control2 was used in the study and thus it is not possible to assess the magnitude of aversiveness. In Raj and Gregory’s study, the pigs could enter the CO2 environment voluntarily, whereas in the present study the animals were subjected to forceful handling if they refused to walk towards and enter the CO stunner crate. This may have masked some2
of the difference between the control treatment and the CO treatment in the present2
study, as walking into the stunner crate may have been a choice between two negative stimuli and may have increased the motivation to enter the stunner crate. However, in
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the study by Raj and Gregory 1995 the smell of CO may have caused a suppression2
in appetite, which may have reduced the motivation to enter the CO2 environment voluntarily in that study. In our study, pigs showed no discernible aversion to a brief exposure to 60% CO . However, it is possible that CO becomes more aversive with2 2
longer exposure, possibly due to more severe hyperventilation andror a build up of pungent gases in the lungs. It is also possible that the method of aversion learning used in the present study may not be able to distinguish between mild aversion and the control treatment.
The results of this study may have been affected by the properties of the stimuli. An electric shock with a prodder was a brief, intense tactile stimulus, while the exposure to CO2 gas involved a gradual olfactory stimulus. It is possible that the element of surprise, and the resulting fear response, contributed to the aversiveness of the electric prodder. Although these properties are inherent to the stimuli, they may have contributed to a difference in recognition of the stunner crate as the place of a negative treatment. Aversion learning has been used by several authors to test the aversiveness of
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handling methods and other treatments. In studies by Rushen 1986 and Rushen and
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Congdon 1987 , sheep were repeatedly exposed to aversive treatments restraint,
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increased with each exposure for about five exposures. It was thought that sheep may require several exposures to an aversive stimulus to be able to predict what will happen at the end of the race way in the treatment area. Although the pigs in this study were exposed to the aversive stimulus only once, a similar increase in time to re-enter the crate over several sessions was seen in the current study in pigs that received the prodder treatment. Additional exposure to the raceway after treatment may be required for the animals to learn to associate the start of the raceway with what will happen at the end of the raceway, even if the treatment stimulus is no longer present. It appeared that most pigs that were exposed to the prodder during session 0 moved easily through the raceway during the next session, only to baulk just before the entry to the CO crate.2
During subsequent sessions ease of movement through the race appeared to be affected from the start of the raceway. It is possible that repeated exposures may have increased the sensitivity of the current experiment to detect differences. However, it is also possible that when using multiple exposures, the aversiveness of multiple exposures is
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measured i.e., treatment may become more aversive with experience . Nevertheless, this study showed that an electric shock is considerably more aversive than exposure to CO .2
The results of experiment 3 indicate that the aversion to the V-restrainer belt and the CO crate were not significantly different, although pigs were more hesitant to enter the2
CO crate on first presentation. However, components of the systems tested differed.2
For example, the CO crate was more enclosed than the V-restrainer, the CO crate2 2 involved a step down whereas the V-restrainer was entered via a ramp sloping upwards, etc. Thus, many components of the stunning system can influence the aversiveness of a system as a whole. More research on the separate components of raceways and stunning units is needed to improve design and to minimize stress on pigs during the slaughter
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process. Barton-Gade et al. 1990 found that stressed pigs often react violently to restraint, while behavioural differences between restrained and unrestrained pigs are minor when they were less stressed. In the current experiment, pigs were moved in a quiet manner, with minimal negative handling, to minimize stress. It is possible that the
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CO stunning crate in which pigs are usually unrestrained may be a better system than2
the V-restrainer in commercial systems where pigs are likely to be stressed. Electric prodders are widely used at abattoirs to move pigs along single file raceways. As this study has shown, the use of electric prodders is highly aversive to pigs, making their use a welfare concern. Improved designs of raceways and education of abattoir workers will reduce the need for the use of electric prodders to move pigs and hence greatly improve welfare of pigs during the slaughtering process. The impact of CO2 stunning and electrical stunning on the welfare of pigs may depend on conditions at the abattoir. However, the present experiments have shown that CO per se is not highly aversive to2 pigs.
Acknowledgements
References
D’Souza, D.N., Warner, R.D., Leury, B.J., Dunshea, F.R., 1998. The effect of dietary Magnesium Aspartate Supplementation on pork quality. J. Anim. Sci. 76, 104–109.
Forslid, A., 1987. Transient neocortical, hippocampal and amygdaloid EEG silence induced by one minute inhalation of high concentration of carbon dioxide in swine. Acta Phys. Scand. 130, 1–10.
Grandin, T., 1988. Possible genetic effect on pig’s reaction to CO stunning. In: Proceedings 34th Interna-2 tional Congress of Meat Science and Technology. CSRIO Meat Research Laboratory, Cannon Hill, Queensland, Australia.
Gregory, N.G., Raj, A.B.M., Audsley, A.R.S., Daly, C.C., 1990. Effect of CO on man. Fleischwirtschaft 70,2 1173–1174.
Raj, A.B.M., Gregory, N.G., 1995. Welfare implications of the gas stunning of pigs: 1. Determination of aversion to the initial inhalation of carbon dioxide or argon. Anim. Welf. 4, 273–280.
Rushen, J., 1986. Aversion of sheep to electro-immobilization and physical restraint. Appl. Anim. Behav. Sci. 15, 315–324.
Rushen, J., Congdon, P., 1987. Electro-immobilization of sheep may not reduce the aversiveness of a painful treatment. Vet. Rec. 120, 37.
