JFS: Food Engineering and Physical Properties

The Effect of Stunning Methods on

Rigor Mortis and Texture Properties of
Atlantic Salmon (Salmo Salar )
B. ROTH, D. MOELLER, J.O. VELAND, A. IMSLAND, AND E. SLINDE

ABSTRACT: Shear force and rigor mortis were used to evaluate the post-mortem changes of muscle texture in
Atlantic salmon (Salmo salar). The fish were either stunned with carbon dioxide (CO2), electricity, or percussion
prior to slaughter. The pre-mortem stress during CO2 stunning resulted in an earlier onset and resolution of rigor
mortis, and accelerated post-mortem softening of the muscle tissue as compared to the other stunning methods. No
significant differences, either in development of rigor mortis or shear force, were seen between fish that were
stunned with electricity or by percussion. Consequently electricity can be used for stunning fish prior to slaughter.
Keywords: Atlantic salmon, stunning, slaughter, rigor mortis, texture

Introduction ferent stunning methods and post-mor- ning methods (CO2, electricity, and per-
Food Engineering and Physical Properties

F ARMED ATLANTIC SALMON (SALMO-

salar) are slaughtered in a way that in-
volves a high degree of stress through
gathering, hauling, stunning and bleed-
ing. Most stressful is the use of carbon di-
oxide (CO2) for stunning, which caused
panic and flight reactions due to the acidic
and hypoxic environment. Accordingly,
the fish will quickly deplete high-energy
phosphogens and give rise to an earlier
onset of rigor mortis (Thomas and others
1999). Further, it has been reported that
an earlier onset of rigor mortis, caused by
stress, can provide greater muscle contrac-
tile tensions and shortening than ob-
served in unstressed stated fish (Nakaya-
ma and others 1999). In rainbow trout
(Oncorhynchus mykiss), it has been stated
that the softening of the texture is mainly
caused by weakening of the supporting
pericellular connective tissue (Ando and
others 1995). Consequences of pre-mor-
tem stress are an earlier resolution of rigor
mortis and a softer texture (Nakayama
and others 1996), gaping (Dunajski 1979;
Lavety and others 1988), and loss of shelf
life (Lowe and others 1993).
One possible way to inhibit pre-mor-
tem stress is to use electrical stunning pri-
or to slaughter. This is widely used within
the broiler industry where it is shown that
electric stunning does delay the post-mor-
tem changes (Raj and others 1995), and
this may be explained by the inhibition of
pre-mortem struggle (Papinaho and oth-
ers 1995). On fish, Azam and others (1989)
and Marx and others (1997) compared dif-
tem change in rainbow trout using CO 2,
electricity, and percussion. Results indi-
cated, in terms of quality, that electrical
stunning did lie in between the other 2
stunning methods. Exposure to electricity
is known to attain some physiological con-
sequences in fish. The tetanus during ex-
posure will deplete high-energy phospho-
gens such as creatine phosphate (PCr)
and adenosine triphosphate (ATP) (Chiba
and others 1990), and carbohydrates such
as glycogen and glucose (Schreck and oth-
ers 1976). The amount of energy con-
sumed in the muscles depends on which
type of electric current is used: direct cur-
rent (DC), pulsed DC (pDC), or alternat-
ing current (AC). Also, electric field
strength (Mitton and McDonald 1994; Bar-
ton and Grosh 1996) and duration (Chiba
and others 1990) are of importance in
stimulating muscle contractions. Robb
and others (2000a) showed that electrical
stimulation of fish muscle did accelerate
the process of rigor mortis. Accordingly, by
minimizing the current duration and field
strength to the thresholds needed to stun
fish, the effect of electrical stimulation on
muscles may be of less importance, and
injuries may be avoided. This gives reason
to believe that use of electrical stunning
prior to slaughter is a satisfactory way of
stunning fish in order to avoid stress and
improve the quality. Furthermore, electri-
cal stunning may be considered more eth-
ical than other stunning methods.
The aim of the present study was to in-
vestigate the effect of the different stun-
cussion) on post-mortem changes of tex-
ture properties in Atlantic salmon. After
stunning, bleeding and gutting, texture
properties were evaluated as shear force
and strength of rigor mortis.
Materials and Methods
The experiment
For shear force analysis, we used a total
of 94 salmon with mean length 68 ± 5 cm
SE. The experiments were performed in
February, and the sea temperature was
6 °C. Shear forces were measured from 12
to 175 hours post-mortem.
In May, a total of 48 salmon with mean
fork length equal to 62 ± 3 cm SE were
used to measure strength of rigor mortis
(rigor index). The sea temperature was
9 °C, and the rigor indexes were then mea-
sured from 0 to 56 hours post-mortem.
For measuring both shear force and rig-
or index, 1 salmon at a time was randomly
removed from its pen and stunned using
CO2, electricity, or percussion. For CO2
stunning, the fish was placed in a tank of
seawater saturated with CO2 for a mini-
mum of 4 min or until the fish was proper-
ly stunned. The CO2 saturation of the tank
started 2 hours prior to the experiments,
and the gas flow was maintained through-
out the entire experiment. For electrical
stunning, we used 1 phase: sinusoidal
50 Hz AC. The current duration was regu-
lated by a time relay and set to 1.5 s. The
fish was placed in a 100 x 30 x 35 cm plexi-
glass tank filled with seawater and elec-

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 Effect of stunning on muscle properties in fish…

Table 1—The internal temperature of Atlantic salmon (Salmo salar) after chill- The potential difference (V ) was mea-
ing in 1 °C seawater for 40 min. Temperature at sea was 13 °C. The fish was sured in root mean square. For percussion,
either live chilled or chilled in the gutted condition. Ice slurry was used during
CO2 stunning. 1 fish at a time was removed from its pen
and immediately hit in the head with a
Mean Mean steel hammer.
Stunning Number length Temperature ± SE
In June, 25 salmon at a sea temperature
method (N) (cm) (°C) of 13 °C and mean fork length equal to 81
cm ± 1 cm SE were stunned using either
CO 2 5 78.2 3.1 ± 0.1
Percussion 5 82.2 3.4 ± 0.3 CO2, electricity, or percussion. The percus-
Electric 6 s 5 79.6 3.7 ± 0.4 sive stun was performed on 2 groups of
Electric 12 s 5 79.5 3.4 ± 0.3 fish, with or without live chilling in 1 °C sea-
Live chilled 5 83.6 2.9 ± 0.3 water for 40 min prior stunning. The electri-
cal stunning was carried out using sinusoi-
trodes 100 cm apart. The electrodes con- rod, covering the whole surface at each dal 1000 Hz AC with field strength equal to
sisted of horizontally aligned steel rods end. The fish was exposed to a homoge- 75 V × m-1, and the fish were electrically
with a distance of 2.5 cm between each nous electric field (E) equal to 175 V × m-1. stunned for either 6 s or 12 s duration. Rigor
indexes were then measured from 0 to 48
hours post-mortem.
After stunning, gill arches were cut, all
salmon were bled in chilled seawater for
40 min, gutted, and then placed in boxes
with crushed ice. The fish was then trans-
ported to a refrigerator and stored at 0 °C
for the entire experiment.

Food Engineering and Physical Properties

Analysis of shear force and rigor
mortis
For preparation of analysis of muscle
shear force, 5 fish from each group were
filleted, and a borer, 25 mm in diameter,
was used to cut out cylindrical muscle
samples in the region of the Norwegian
Quality Cut (NQC). NQC is the epaxial
part of the fillet confined by vertical lines
at the posterior end of the dorsal fin and
the anterior end of the anal fin. The num-
Figure 1a—Measured Warner-Bratzler shear force values (mean ± SE) on muscle ber of samples varied from 4 to 7, depen-
from Atlantic salmon (Salmo salar) stunned either with CO2, electricity, or by
percussion . The shear force was measured at 12, 32, 54, 80, 102, and 175 dent on fish size. For texture measure-
hours post-mortem, and maximum shear force (N) was recorded. ments we used TA-XT2 ® Texture Analyzer
from Stable Micro Systems equipped with
a Warner-Bratzler test cell. The muscle
samples were sliced at a constant speed of
2.0 mm×s-1 with a 3-mm thick, 73 ° angle in-
verted knife. The shear force was deter-
mined by the maximum force (N) record-
ed and the total amount of work ( J) used
to slice through the sample.
The rigor index (I R) was calculated by
the following formula: IR = [(L0 - Lt) / L0] *
100 (Bito and others 1983). L represents, in
cm, the vertical drop of the tale when half
of the fish length was outside a table. L0
represents the vertical drop measured at
the beginning of the experiment, while Lt
represents measurements throughout the
experiment.

Statistical analysis
ANCOVA and multistage categorical re-
Figure 1b—Measured Warner-Bratzler shear force values (mean ± SE) on muscle
from Atlantic salmon (Salmo salar) stunned either with CO2, electricity, or by gression (Sokal and Rohlf 1994) were used
percussion. The shear force was measured at 12, 32, 54, 80, 102, and 175 to test differences in muscle shear force,
hours post-mortem, and the total amount of work (J) used to slice the muscle depending on stunning methods. The fish
was recorded. size was expected to influence the muscle

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 Effect of stunning on muscle properties in fish…

shear strength (Veland and Torrissen
1999), and was therefore included as an in-
dependent variable in multiple regression,
as a covariate in ANCOVA. To compare dif-
ferences of the slope on shear force caused
by different stunning methods, the inde-
pendent variables “stunning methods”
were incorporated in multiple regression as
multistage categorical independent vari-
ables (Sokal and Rohlf 1994). This test al-
lows comparison of more than 2 slopes with
a joint intercept. The stunning methods
were categorized as 0 and 1, separating 1
stunning method from the other 2.
For analysis of rigor index, we used
ANOVA and post-hoc analysis (Sheffels
test of unequal n).
0.05, Sheffels test of unequal n). For fish
stunned with electricity or killed by per-
cussion, there were no difference in the
timing of onset and resolution of rigor
mortis (Figure 2).
Statistical analysis of the results in
Figure 3, showed that CO 2 stunned fish
had a significantly higher rigor index at 6
hours post-mortem than the other stun-
ning methods (P < 0.05, Sheffels test of
unequal n). At 12 hours post-mortem,
both the CO 2 and live chilled fish did
achieve maximum rigor index, while the
fish killed by percussion or electrically
stunned for 6 s did not achieve maximum
rigor index until 24 hours post-mortem
(Figure 3). Fish stunned electrically for a
12 s duration tended to have an earlier
onset of rigor mortis than fish stunned for
a 6 s current duration, but no significant
difference was found in rigor index be-
tween these 2 groups (P > 0.05, Sheffels
test of unequal n).
As seen in Table 1, after chilling in sea-
water and prior to placement in boxes of
ice, there was no significant difference (P >

Results and Discussion

Texture analysis
The results of muscle shear force
(Figure1a and 1b) indicated that the post-
mortem softening of the texture was de-
pendent on stunning method and the
storage time (P < 0.05, ANCOVA). Fish
Food Engineering and Physical Properties

stunned with CO2 had a significantly lower

shear force (Figure 1a), and less work was
required to slice the sample (Figure 1b)
compared to fish stunned either with elec-
tricity or by percussion (P < 0.05, multi-
stage categorical multiple regression and
ANCOVA). The mean shear values mea-
sured as maximum force and work of CO2
stunned fish (Figure 1a and 1b) decreased
rapidly the 1st 54 hours and settled at
about 80 hours post-mortem. Similar Figure 2—Results from rigor mortis measurements on Atlantic salmon (Salmo
salar) after stunning with CO2, electricity, or by percussion. The rigor index
mean shear values from the other 2 stun- (%) was measured at 0, 6, 12, 20, 28, 40, 48, and 56 hours post-mortem (mean
ning methods (Figure 1a and 1b) did not values ± SE).
occur until 175 hours post mortem. No sig-
nificant differences in shear force were
found (P > 0.05, multistage categorical
multiple regression and ANCOVA) be-
tween fish stunned with electricity or by
percussion (Figure 1a and 1b).

Rigor index
Shown in Figure 2 and 3, fish stunned
with CO2 had an earlier onset and resolu-
tion of rigor mortis than the other stun-
ning methods. Maximum rigor index was
achieved within 12 hours among the CO2
stunned fish, while the electrically
stunned fish and fish killed by percus-
sion did not achieve maximum rigor index
until 36 hours (Figure 2) and 24 hours
post-mortem (Figure 3), respectively. Sta-
tistical analysis of the results in Figure 2,
show that CO 2 stunned fish had a signifi-
cantly higher rigor index at 6 to 12 hours
Figure 3—Results from rigor mortis measurements on Atlantic salmon (Salmo
post-mortem and significantly lower rigor
salar) after stunning with CO2, 6 s of electricity, 12 s of electricity, or by per-
index from 28 to 48 hours post-mortem cussion with or without live chilling. The rigor index (%) was measured at 0, 6,
than the 2 other stunning methods (P < 12, 24, and 48 hours post-mortem (mean values ± SE).

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 Effect of stunning on muscle properties in fish…
0.05, t-test) in the internal temperature
between fish that were live chilled or
chilled in gutted condition. The live
chilled fish had a mean internal tempera-
ture of 2.9 °C, while the highest mean tem-
perature was found among the electrical
stunned fish equal to 3.7 °C (Table 1).
Hematomes caused by electrical stun-
ning was observed in 4 fish when 50 Hz AC
was used, providing an injury rate of 11%.
No injuries were seen in fish stunned with
1000 Hz, AC.
Assuming that injuries caused by elec-
trical stunning can be avoided, the use of
electricity is an interesting alternative to
CO 2. For electrically stunned fish, the re-
sults on rigor mortis measurements with
use of 50 Hz AC for 1.5 s (Figure 2) or 1000
Hz AC for 6 s (Figure 3) show no evidence
of an accelerated process of rigor mortis
compared to the unstressed fish killed by
percussion. The use of 12 s current dura-
tion did result in an earlier onset of rigor
mortis compared to the group stunned
with a 6 s electric duration or by percus-
sion (Figure 3). Previous reports by Jerret
and others (1998) and Robb and others
(2000a) showed that electrical stimulation
of fish does accelerate the process of rigor
mortis. Electric shock is known to induce
the primary stress responses in rainbow
trout (Schreck and others 1976; Mesa and
Schreck 1989; Mitton and McDonald 1994;
Barton and Grosh 1996). Further, the stim-
ulation of muscle contractions during ex-
posure to AC or pDC does require energy
promoting glycolysis and depletion of ATP
and PCr levels over time (Chiba and oth-
ers 1990; Mitton and McDonald 1994).
This can explain the rigor indexes seen for
the electrical stunned fish in Figure 2 and
3. The use of 50 Hz AC with current dura-
tion at 1.5 s (Figure 2) and 1000 Hz AC at 6
s (Figure 3) seems to represent very short
incidents of muscle stimulation. However,
when the current duration was prolonged
to 12 s (Figure 3), an effect of muscle stim-
ulation was shown by an earlier onset of
rigor mortis.
On texture analysis, CO2 stunned fish
had a sharper decease of maximum shear
force (Figure 1a) and work to slice the mus-
cle sample (Figure 1b) than both the elec-
trical stunned fish and the unstressed fish
killed by percussion. These results do
show that the pre-mortem muscle activity
in fish does contribute to a softer texture.
However, the softening of the muscle tex-
ture in CO2 stunned fish was rather rapid.
As seen in Figure 1b, the work needed to
slice the sample in CO 2 stunned fish was
distinctly lower already at the beginning
of the measurements, 12 hours post-mor-
jfsv67n4p1462-1466ms20010317-BW.P65 1465
tem. This gives reason to speculate if the
softening of the texture in CO2 stunned
fish was directly caused by self injuring
muscle contractions during flight reac-
tions, or if it was caused by acceleration of
rigor mortis and the post-mortem tender-
ization process.
It is shown on poultry that electric
stunning does improve the quality mea-
sured as delay of rigor mortis, higher mus-
cle pH values and more firm texture (Pap-
inaho and others 1995; Raj and others
1995). However, these results were diffi-
cult to compare with fish, since the mor-
phological structures in poultry and fish
muscle are quite different (Dunajski
1979).
Previous studies show that stress with
exercise prior to death does accelerate the
onset and resolution of rigor mortis (Na-
kayama and others 1996; Thomas and oth-
ers 1999). This corresponds well with the
results on CO 2 stunning (Figure 2 and 3).
Salmon reaction to the sudden exposure
to a hypoxic environment is panic, fol-
lowed by a 3 to 4 minutes flight reaction
before they are properly stunned or ex-
hausted (Robb and others 2000b). The
flight reaction will, in this case, force
anaerobic glycolysis, accumulate lactate,
and deplete ATP and PCr within the mus-
cles, generating an earlier onset of rigor
mortis.
Comparing the development of rigor
mortis between Figure 2 and 3 show that
the fish stunned with CO2 and percussion
in Figure 3 do have an accelerated rigor
process compared to the fish in Figure 2.
In both cases, the fish were starved, trans-
ported and rested prior to slaughter. The
difference was the season at slaughter.
Fish in Figure 2 were slaughtered in May
when the temperature at sea was 4 °C less,
and they were 20 cm shorter than the fish
slaughtered in July (Figure 3). What im-
pact the temperature and fish size has on
the development of rigor mortis is, at
present, unclear. Previous studies regard-
ing live chilling of salmon (Skjervold and
others 1999; Skjervold and others 2001)
have shown that low temperature pre-
mortem does delay the onset of rigor mor-
tis. Our results on live chilling (Figure 3) in-
dicate stress within the fish, observed by
an earlier onset of rigor mortis. Skjervold
and others (2001) did show that live chill-
ing induces the primary stress responses
within fish, but the delayed onset of rigor
mortis is mainly caused by low internal
temperature at slaughter. As seen in Table
1, the internal temperature in live chilled
fish was insignificantly lower than that in
fish that were chilled in the gutted condi-
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5/30/2002, 3:59 PM
tion. This indicates that the early onset of
rigor mortis observed among live chilled
fish (Figure 3), was likely to be caused by
the release of the secondary stress re-
sponses.
Conclusion
P RE-MORTEM HANDLING AND STUN-
ning method influences the process of
rigor mortis and post-mortem softening of
the texture. In terms of quality, the use of
electricity and percussion are the most
suitable methods of stunning fish prior to
slaughter when compared to stunning
with CO2.
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Authors are with the Dept. of Fisheries and Marine
Biology, Univ. of Bergen, P.O. Box 20, N-5020
Bergen, Norway. Author Slinde is with the Institute
of Marine Research, P.O. Box 1870, Nordnes, N-
5005 Bergen, Norway. Direct inquiries to author
Roth, Dept. of Fisheries and Marine Biology, Univ.
of Bergen, Hoyteknologisenteret i Bergen, N-5020
Bergen, Norway. (E-mail: Bjorn.Roth@ifm.uib.no).