Aquaculture Aquaculture 149 (1997) 243-252 Handling stress and water quality during live transportation and slaughter of Atlantic salmon ( SaZmo sazar) Ulf Erikson a, Trygve Sigholt a* *, Aina Seland b a SINTEF Applied Chemistry, Aquaculture Centre, N-7034 Trondheim, Norway b SINTEF Hydrotechnicai Laborator?; (NHL), N-7034 Trondheim, Norway Accepted 5 September 1996 Abstract Atlantic salmon (Sulmo s&r), mean weight 5.1 kg, were transported live for 1.5 h by a well-boat (fish density 125 kg II-~) from the seacage to a fish processing plant and then kept in the well-boat for 4 h prior to slaughter. Anaerobic white muscle activity due to handling stress during fish loading at the cage, after shipment immediately before slaughter, and after the fish had passed the slaughter line, was evaluated using high-energy phosphates and IMP, the [ATPLIMP] ratio, adenylate energy charge together with pH and redox potential measured directly in the muscle. Water quality parameters, pH, salinity, temperature, dissolved oxygen, carbon dioxide, total carbonate carbon, total alkalinity, ammonia and ammonium were monitored at the cage, during shipment, and in the carbon dioxide anaesthesia tank during commercial fish slaughter. No dramatic effects of handling stress were found, indicating that transport and slaughtering did not have an adverse effect on flesh quality. The results were explained by the ability of the well-boat to maintain good seawater quality during transport, to a quick bulk netting of the fish from well-boat to the slaughter line and to an efficiently run carbon dioxide anaesthesia-tank that minimised struggling prior to killing. Keywords: Salmo salor; Stress; Muscle; Water quality; Transportation * Corresponding author. Tel.: +4773.596373; fax: +4773596363; e-mail: [email protected]. 0044.8486/97/$17.00 Copyright 0 1997 Elsevier Science B.V. All rights reserved PII SOO44-8486(96)01453-6
Transcript
Aquaculture
Aquaculture 149 (1997) 243-252
Handling stress and water quality during live transportation and slaughter of Atlantic salmon
( SaZmo sazar)
Ulf Erikson a, Trygve Sigholt a* * , Aina Seland b a SINTEF Applied Chemistry, Aquaculture Centre, N-7034 Trondheim, Norway
b SINTEF Hydrotechnicai Laborator?; (NHL), N-7034 Trondheim, Norway
Accepted 5 September 1996
Abstract
Atlantic salmon (Sulmo s&r), mean weight 5.1 kg, were transported live for 1.5 h by a
well-boat (fish density 125 kg II-~) from the seacage to a fish processing plant and then kept in the well-boat for 4 h prior to slaughter. Anaerobic white muscle activity due to handling stress during fish loading at the cage, after shipment immediately before slaughter, and after the fish had passed the slaughter line, was evaluated using high-energy phosphates and IMP, the [ATPLIMP] ratio, adenylate energy charge together with pH and redox potential measured directly in the muscle. Water quality parameters, pH, salinity, temperature, dissolved oxygen, carbon dioxide, total carbonate carbon, total alkalinity, ammonia and ammonium were monitored at the cage, during shipment, and in the carbon dioxide anaesthesia tank during commercial fish slaughter. No dramatic effects of handling stress were found, indicating that transport and slaughtering did not have an adverse effect on flesh quality. The results were explained by the ability of the well-boat to maintain good seawater quality during transport, to a quick bulk netting of the fish from well-boat to the slaughter line and to an efficiently run carbon dioxide anaesthesia-tank that minimised struggling prior to killing.
Keywords: Salmo salor; Stress; Muscle; Water quality; Transportation
0044.8486/97/$17.00 Copyright 0 1997 Elsevier Science B.V. All rights reserved
PII SOO44-8486(96)01453-6
244 U. Erikson et al. /Aquaculture 149 (1997) 243-252
1. Introduction
Production of farmed Atlantic salmon (Sulmo s&r) in Norway normally includes transport of live fish in specially designed well-boats from the seacages to the plants where slaughter and processing take place. Transport at high densities, loading and unloading, capture, netting or pumping of the fish are all adverse stimuli that may cause numerous physiological reactions. During transport, stress may also be caused by low levels of oxygen or poor water quality due to inadequate water exchange that causes accumulation of excreted carbon dioxide and ammonia.
It has previously been shown that transport of salmonids for up to 11 h at loading densities of 69-170 kg me3 had only a minor effect on physiological responses (McDonald et al., 1993) and that the capture and loading of red drum (Sciuenops ocellutus~ for 5.5 h are more stressful than the transport itself (Robertson et al., 1988). Specker and Schreck (1980) found raised levels of plasma corticosteroids when trans- porting smolting coho salmon (Oncorhynchus kisutch) at densities of 12-120 kg mm3 for 4-12 h, but also in this case the greatest stress occurred during loading and during the first few hours of transport. Ostenfeld et al. (1995) reported that the effects on muscle metabolites and fillet texture after road haulage of rainbow trout (Oncorhynchus
mykiss) for 10.5 h at 167 kg rn- 3 had a limited effect on flesh quality. Stress and muscle activity during the transport, netting and anaesthesia of fish may
shorten the time to onset of rigor morns, which is essentially triggered by depletion of glycogen and ATP in muscle cells (Hultin, 1985). Handling and processing of fish during rigor mortis can result in a loss of quality and lower fillet yield (La&y, 1984). The pre-rigor period must therefore be long enough to ensure that bleeding, gutting, washing, chilling and packing all take place before the onset of rigor morns. Ante mortem handling stress also has adverse effects on product quality, such as reducing fish freshness (Izquierdo-Pulido et al., 1992; Lowe et al., 1993) and softening muscle texture (Ando et al., 1992; Nakayama et al., 1994).
The objective of this study was to assess the energy status of white muscle in large commercial size salmon before and after well-boat transport, and before and after going through a commercial slaughter line. Water quality during the well-boat transport and in the anaesthesia tank was also monitored. By making these comparisons, we hoped to identify critical points in the process at which the flesh quality of the final product might be reduced due to handling stress.
2. Materials and methods
2.1. Experiment& fish
Atlantic salmon (Sulmo s&r) were transferred to the seacage as l-year smolts approximately 2 years before the experiment was conducted. The fish were fed according to the manufacturer’s recommendations with a commercial diet (Ewos Gull) containing 40% protein and 30% fat during the 6 months prior to harvesting. The fish were starved for 12 days before slaughter, by which time their mean weight was
U. Erikson et al. /Aquaculture 149 (1997) 243-252 245
5.1 & 1.1 kg (n = 33). The mean total fat content in a section of the muscle excised
under the dorsal fin, including red muscle and belly flap, was 19 f 2% (n = 12) as determined using a modified version of the method of Bligh and Dyer (Hardy and Keay, 1972).
2.2. Cage and transportation
The fish (25 tons) were netted from the cage (4100 m3) and transferred to the well-boat within 90 min. The well-boat, which had a total load capacity of 200 m3, was equipped with two pumps each with a capacity of 750 m3 hh’, with six 14 in. valves in the forward end and six 14 in. valves in the after end of the hold, and equipment for water oxygenation. During transportation to the plant (26 km, 90 min) at a fish density of 125 kg me3 all the valves were left open for constant circulation of fresh seawater. The operation took place under excellent weather conditions and in a calm sea.
2.3. Quay and slaughtering
On arrival at the plant quay, the front valves were left open and the water was pumped (about 1000 m3 hh ‘) out from the aft of the hold. The slaughtering process started 4 h after arrival, when the fish were netted and lifted in a water-filled net to a stainless steel platform. The fish slid from the platform into a tank (2 m3) containing seawater through which CO,(g) was bubbled to anaesthetise the fish. Then the gills were cut and the fish were bled in a tank (9 m3> containing circulating seawater. The rest of the slaughter line consisted of gutting, washing, chilling, weighing and packing in ice in styropore boxes.
2.4. Water quality analysis
Water temperature, dissolved oxygen, and pH were measured directly before trans- port in the cage, during transport in the well-boat and at the plant during anaesthesia in the carbon dioxide tank when the fish were slaughtered. In addition, water samples were taken and stored in gas-tight bottles for 3-4 days before analysis for dissolved oxygen and carbon dioxide, salinity (S), total alkalinity (TA) and total ammonia nitrogen (TAN = (NH:-N) + (NH,-N)). Dissolved oxygen analysis was based on the Winkler method (Norwegian Standard, 1988).
Seawater pH was measured using a WTW-pH 192 meter and salinity by a WTW- LF537 meter. TA was analysed by acid titration according to Norwegian Standard (198 1) and carbon dioxide was analysed as total carbonate carbon, defined as C, = H,CO, + HCO; + CO:- using a Tecator Flow Injection Analyzer (FIA system 5010) as described in Tecator Application Notes ASN 66-01/83 and ASN 66-02/83.
Dissolved carbon dioxide was then calculated from C,, pH and the carbonate equilibrium constants given by Gieskes (1974).
TAN content was also determined by the FIA method according to Tecator Applica- tion Note ASN 50-06/9 1. The concentrations of NH 3 and NH: were then calculated on the basis of the analysed TAN values, pH and the equilibrium constant K, (Bower and
246 (1. Erikson et al. /Aquaculture 149 (19971243-252
Bidwell, 1978). All water-quality parameters analysed by the FIA method were assayed in duplicate and reported as means.
2.5. Assessment of handling stress
Before transport, 12 fish were netted individually at the cage and killed by a blow to the head within 20 s. Samples (about 3 g) of epaxial white muscle were excised and freeze-clamped within 25 s using liquid nitrogen pre-cooled Al-tongs (Borjeson and Fellenius, 1976) and were subsequently stored in liquid nitrogen and later at - 80°C until HPLC analysis. As the sampling took place, the white muscle pH and redox potential were recorded.
The sampling protocol was repeated at the quay, where the fish were netted individually directly from the well-boat 4 h after arrival and immediately before the unloading and slaughtering of the fish started.
The fish were transferred to the slaughter line and the stunning tank within 45 s in batches, using a landing net. Stunning was effective within l-2 min. The fish remained in the tank for at most 5 min and were subsequently bled for at least 20 min. The experimental fish were marked individually by opercular clips after being anaesthetised and collected at the end of the slaughter line, 80 f 21 min post mortem. White muscle sampling was carried out immediately as already described.
2.6. Fish muscle analysis
2.6. I. High energy phosphates After freeze drying (Hetosicc, mod. CD 13-l) the samples were analysed using the
HPLC method of Sellevold et al. (1986) with a few minor modifications. Stainless steel containers including steel balls were pre-cooled in liquid nitrogen, filled with freeze-dried muscle sample and attached to a vibratory mill (Retsch, type MM-2) where the samples were powdered (20 s). Ice-cold perchloric acid (500 p.1, 0.42 M) was added to the powdered tissue (5-10 mg) and whirlmixed periodically for 10 min. The extracts were centrifuged (1300 X g, 5 min, - 10°C) and the supematants (400 pl) neutralised by addition of ice-cold K,CO, (220 pl, 0.36 M). After 10 min in ice, the extracts were centrifuged (1300 X g, 5 min, - 10°C) and the supematants assayed. The HPLC system consisted of a Rheodyne 710-SNR injector with a 20 pl loop, a ICI mod. LC 1100 pump, a UV/VIS ICI mod. LC 1200 detector, a ICI DP 800 Chromatography Data Station and a Supelcosil LC-18-T (150 X 4.6 mm) column. The microfiltered isocratic mobile phase, adjusted to pH 6.25, consisted of KH,PO, (215 mM), tetrabutylammo- nium hydrogen sulphate (TBAHS, 2.3 mM) and acetonitrile (3.5%). The flow rate was 1.3 ml mini’ and the samples were compared with Sigma external standards of the relevant metabolites and related degradation products.
The effects of handling stress are expressed in terms of mean concentrations of PCr, ATP, and IMP (pm01 g-’ dry weight), the [ATP:IMP] ratio based on group average values, and adenylate energy charge (AEC = (0.5 ADP + ATP)/(AMP + ADP + ATP)) (Atkinson, 1968; Reinert and Hohreiter, 1984).
U. Erikson et al. /Aquaculture 149 C 1997) 243-252 247
2.6.2. pH White muscle pH was measured directly using a Radiometer type GK 2713 electrode
connected to a type pHM 80 meter.
2.6.3. Redox potential
White muscle redox potential was measured using a directly inserted platinum electrode (length 20 mm, diameter 3 mm) vs. a Radiometer REF201 Ag/AgCl reference electrode, both in a Teflon holder. The results (in mV) were measured using a multimeter (Fluke mod. 27) and are reported relative to the hydrogen scale (E,).
2.7. Statistics
Throughout, values are reported as means k 1 SD. Differences between treatments, i.e. fish at cage, at quay and slaughtered, were tested using a one-way ANOVA followed by Tukey’s test using SYSTAT ver. 5.04 (Wilkinson et al., 1992). A significance level of 0.05 was chosen.
3. Results
Water-quality parameters in the cage before transport, in the well-boat from the time of loading, during transport and at the quay, and in the carbon dioxide anaesthesia tank during the process of slaughtering, are shown in Table 1. No marked changes in water quality took place during transport compared with the cage, which was situated at a
Table 1
Seawater quality at cage, during shipment and in carbon dioxide anaesthesia tank at slaughter
b Immediately after individual netting and killing before transportation.
’ After individual netting from the well-boat and immediate killing, 4 h after transportation.
d After slaughter, 80+ 21 min post mortem.
* P < 0.05.
location with good water exchange. The conditions in the anaesthesia tank were different, with pH and oxygen values roughly half of those in the well-boat, while the carbon dioxide content was more than a thousand times higher than the saturation value of 0.7 mg CO, 1~ ‘. The TAN content was considerably higher and at this low pH the TAN is essentially equal to NH:. The salinity and total alkalinity did not differ from cage and transport conditions.
The mean white muscle pH values of the three groups are shown in Table 2. Only the fish that had passed the slaughter line had a significantly different (lower) value, whereas none of the mean redox potentials (Table 2) were significantly different. The mean concentrations of PCr, ATP, struggle-induced IMP, group average [ATPIMP] ratio and the mean AEC values are shown in Table 2. The fish at the quay were somewhat less stressed than the other two groups, as shown by significantly higher levels of PCr and ATP. No significant difference in IMP was found.
4. Discussion
None of the water-quality parameters (Table 1) suggested that adverse water quality prevailed at any time during well-boat transport. For instance, Alabaster et al. (1979) reported ammonium 24 h LC,, values of 0.12 and 0.28 mg 1-l in Atlantic salmon in
saltwater, indicating our ammonia concentrations were well below toxic levels. No mortality was observed and the fish seemed calm throughout the transportation,
except during loading and unloading. The weather conditions during transport were optimal, i.e. the sea was absolutely calm. Often, the weather conditions on the Norwegian coast can be rather rough. Therefore, the transport described here may not be typical. Under good weather conditions similar to those reported here, we have obtained comparable results concerning the white muscle handling stress parameters on other occasions (Berg et al., 1997). Thus, these results are probably representative of good transport conditions.
The levels of oxygen (3.0 mg 0, l- ‘) and carbon dioxide in the anaesthesia tank
U. Erikson et al. /Aquaculture 149 (1997) 243-252 249
seemed to be sufficient to immobilise the salmon quickly without causing severe anaerobic metabolism in the white muscle or suffocating the fish due to lack of oxygen. By comparison, the critical level of dissolved oxygen in freshwater for coho (Oncor- hynchus kisurch) and sockeye (0. nerku) salmon ranges from 4.0 to 4.5 mg OZ 1-l at 15°C (Brett and Blackbum, 1981). The carbon dioxide content calculated as partial pressure was 284 mm Hg (7°C S = 35%0) which is comparable to the CO, value of 250 mm Hg used for non-lethal anaesthesia of carp (Cyprinus c&o) (Yoshikawa et al.,
1991). The elevated TAN content (entirely in the form of ammonium at this low pH), can be
ascribed to a higher fish metabolic rate in a relatively small tank volume. The white muscle pH in the cage and at the quayside are comparable to those of
rested salmonids (Booth et al., 1995; Wang et al., 1994), indicating that rapid netting and killing of fish of this size did not seriously affect muscle pH. During slaughter, including a possible contribution from about 80 min of post mortem glycogen catabolism, the pH was reduced by almost 0.4 units, which is about 0.2-0.3 units higher than is usually reported for exhausted salmonids (Booth et al., 1995; Ferguson et al., 1993; Tang and Boutilier, 1991). This suggests that struggling during bulk netting and in the anaesthesia tank was moderate, which in turn indicated efficient anaesthesia.
The positive redox potentials are consistent with oxidising conditions prevailing in the fish muscle and although no statistically significant difference between treatments was found, the mean value in the fish sampled from the quay was 20 mV higher than the other treatments, which might be ascribed to lower muscle activity of the fish in this group when being sampled. Furthermore, the redox potentials are consistent with those measured previously (Eh = + 100 to + 300 mV> in very fresh fish (Huss and Larsen, 1979). When adjusted to the biological scale (pH 7.0), the mean redox potentials were in the vicinity of - 210 mV which is relatively close, for instance, to the standard potential of the pyruvate/lactate couple at - 190 mV. However, the observed potentials are probably difficult to interpret accurately quantitatively since what we observed was probably a ‘mixed potential’ originating from several redox systems.
The HEP values (Table 2) expressed as the [PCr:ATP] ratios in the cage, at the quay and after slaughter were 2.0, 2.8 and 1.5, respectively. This is only slightly lower than values reported for rested fish which range from 3.3 (Dobson and Hochachka, 1987) to 4.3 (Van Raaij et al., 1994). The IMP content in the muscle was 2.0, 1.0 and 1.3 pmol g- ’ (dry weight) in the cage, at the quay and after slaughter, respectively. These are somewhat higher than the value of about 0.1 kmol g- ’ (dry weight) reported in rested rainbow trout white muscle (Van Raaij et al., 1994). The [ATPIMP] ratio after slaughter (9.5), however, was higher than in the cage (5.9) but lower than at the quay (14.5).
The mean AEC of the treatments, ranging from 0.91 to 0.94 were not significantly different and are all comparable to 0.93 (Van Raaij et al., 1994) and 0.95 (Schulte et al., 1992) in rested rainbow trout white muscle. In comparison, in the latter case it was reported that the AEC was reduced to 0.84 when the fish were exercised to exhaustion for 25-30 min.
As a summary of the assessment of white muscle handling stress, it seemed that in all treatments, the fish were little stressed, i.e. no prolonged struggling had apparently taken place. Quick netting and killing of salmon did not seem to markedly affect the adenylate
250 U, Erikson et al./Aquaculture 149 (1997) 243-252
system, because at this time-scale (few seconds) the ATP is replenished by PCr (Erikson et al., 1997) and only limited amounts of IMP are formed by the AMP deaminase reaction, resulting in a stabilisation of the AEC (Chapman and Atkinson, 1973). Even though only PCr and ATP at the quay were significantly different from the other treatments, the mean AEC and redox potential values were higher and the mean IMP value was correspondingly lower in this group. These values, being closer to those of rested fish, might be ascribed to a possible recovery effect during the 4 h that the well-boat was at the quayside before sampling. This is within the recovery time of about 2 h in the case of the adenylate system and PCr in Atlantic salmon white muscle when recovering from exhaustive exercise (Booth et al., 1995). Another possibility is that during sampling at the quay, the fish clearly seemed to be quieter than at the cage when being netted individually. This behaviour might have been an effect of the transport that cannot be explained by the measured water quality parameters (Table 1).
As judged by the indicators of anaerobic metabolism, the slaughtered fish appeared, somewhat surprisingly, to be relatively little affected by handling stress (including 80 min post mortem catabolism before sampling) during slaughtering. In two comparable experiments conducted at two different commercial plants, the effects of handling stress were substantial with mean f SD (n = 14-18) PCr, ATP, IMP, [ATP:IMP], AEC and pH values (metabolites in pmol g-’ (dry weight)) of 7.1 * 6.0 and 3.9 f 5.1; 8.0 !c 4.5 and 9.1 f 6.4; 10.2 & 4.5 and 6.0 5 5.7; 0.8 and 1.5; 0.80 f 0.12 and 0.80 &- 0.21; 6.4 &- 0.1 and 6.8 * 0.1, respectively (unpublished data). In another comparable experi- ment (n = 10) the mean values (pH not measured) were 2.3 + 1.9, 3.3 t_ 3.9, 10.3 + 6.6, 0.3, and 0.66 rfr 0.21, respectively (Berg et al., 1997). These data suggest that salmon are usually more exhausted at the time of death during commercial slaughter than in the experiment reported here. These differences are most likely to be dependent on differences in the routines during transfer of fish from the well-boat to the slaughter-line and the efficiency of the anaesthesia/stunning routines. Rapid and careful bulk netting using liberal amounts of water as in this study, seems to be an adequate way of minimising the detrimental effects of handling stress.
Since the onset of rigor mortis occurs when the ATP in the muscle is nearly depleted, and since the ATP content of the fish that had passed the processing line was relatively high, the plant evaluated here was able to benefit by processing and packing the fish before the onset of rigor. Another important possible benefit that could be ascribed the modest handling stress observed here, was the avoidance of a strong rigor tension in stressed fish (Nakayama et al., 1994) resulting in tenderisation of the muscle (Ando et al., 1992) and softer muscle texture (Izquierdo-Pulido et al., 1992; Sigholt et al., 1997). Furthermore, IMP is retained longer post mortem in the muscle of unstressed fish, thus delaying the formation of hypoxanthine. One consequence of this is lower K-values for unstressed fish for several days when stored in ice (Izquierdo-Pulido et al., 1992; Erikson et al., 1997).
Acknowledgements
The authors wish to thank the crew of M/S Froytrans and the staff of Flora Fiskeindustri A/S for their generous help during this study. This work was carried out
U. Erikson et al. /Aquaculture 149 (1997) 243-252 251
as a part of the SINTEF Strategic Technology Programme of Aquaculture and was financially supported by the Research Council of Norway (NTNF project 26877).
References
Alabaster, J.S., Shurben. D.G. and Knowles, G., 1979. The effect of dissolved oxygen and salinity on the
toxicity of ammonia to smelts of salmon (S&to s&r L.). J. Fish Biol., 15: 705-712.
Ando, M., Toyohara, H. and Sakaguchi, M., 1992. Post-mortem tenderization of rainbow trout muscle caused
by the disintegration of collagen fibers in the pericellular connective tissue. Nippon Suisan Gakkaishi, 58:
567-570.
Atkinson, D., 1968. The energy charge of the adenylate pool as a regulatory parameter. Interaction with
feedback modifiers. Biochemistry, 7: 4030-4034.
Berg, T., Erikson, U. and Nordtvedt, T.S., 1997. Rigor mortis assessment in Atlantic salmon (Salmo salor)
and effects of stress. J. Food Sci. (in press).
Booth, R.K., Kieffer, J.D., Davidson, K., Bielak, A.T. and Tufts, B.L., 1995. Effects of late-season catch and
release angling on anaerobic metabolism, acid-base status, survival, and gamete viability in wild Atlantic
salmon (Sa[mn s&r). Can. J. Fish. Aquat. Sci., 52: 283-290.
Bower, C.E. and Bidwell, J.P., 1978. Ionization of ammonia in seawater. Effects of temperature, pH and
salinity. J. Fish. Res. Board Can., 35: 1012-1016.
Brett, J.R. and Blackbum, J.M., 1981. Oxygen requirements for growth of young coho (Oncorhynchus kisutch)
and sockeye (0. nerku) salmon at 15°C. Can. J. Fish. Aquat. Sci., 38: 399-404.
Borjeson, H. and Fellenius, E., 1976. Towards a valid technique of sampling fish muscle to determine redox
substrates. Acta Physiol. Stand., 96: 202-206.
Chapman, A.G. and Atkinson, D.E., 1973. Stabilization of adenylate energy charge by the adenylate
deaminase reaction. J. Biol. Chem., 248: 8309-8312.
Dobson, G.P. and Hochachka, P.W., 1987. Role of glycolysis in adenylate depletion and repletion during work
and recovery in teleost white muscle. J. Exp. Biol., 129: 125-140.
Erikson, U., Beyer, A.R. and Sigholt, T., 1997. Muscle high-energy phosphates and stress affect K-values
during ice storage of Atlantic salmon (Salvo s&r). J. Food Sci., 62: 1-5.
Ferguson, R.A., Kieffer, J.D. and Tufts, B.L., 1993. The effects of body size on the acid-base and metabolite status in the white muscle of rainbow trout before and after exhaustive exercise. J. Exp. Biol., 180:
195-207.
Gieskes, J.M., 1974. The alkalinity-total carbon dioxide system in seawater. In: E.D. Goldberg (Editor), The
Sea, Vol. 5, Marine Chemistry. John Wiley, New York, pp. 123-151.
Hardy, R. and Keay, J.N., 1972. Seasonal variations in chemical composition of Cornish mackerel Scorn&r
scombus CL.1 with detailed reference to the lipids. J. Food Technol., 7: 125-137.
Huss, H.H. and Larsen, A., 1979. The post mortem changes in the oxidation-reduction potential of fish muscle and internal organs. In: K. Sobolenska-Ceronik, E. Ceronik and S. Zaleski (Editors), Food as an Ecological
Environment for Pathogenic and Index-Organisms. Ars Polonia, Poland, pp. 265-279.
Izquierdo-Pulido, M.L.. Hatae, K. and Haard, N.F., 1992. Nucleotide catabolism and changes in texture
indices during ice storage of cultured sturgeon, Acipenser transmontanus. J. Food Biochem., 16: 173-192.
LavCty. J., 1984. Gaping in farmed salmon and trout. Torry Advisory Note No. 90, Tony Research Station, Aberdeen.
Lowe, T.E., Ryder, J.M., Carragher, J.F. and Wells, R.M.G., 1993. Flesh quality in snapper, Pagrus auratus,
affected by capture stress. J. Food Sci., 58: 770-773, 796.
McDonald, D.G., Goldstein, M.D. and Mitton, C., 1993. Responses of hatchery-reared brook trout, lake trout, and splake to transport stress. Trans. Am. Fish. Sot., 122: 1127-I 138.
Nakayama, T., Toyoda, T. and Ooi, A., 1994. Physical property of carp muscle during rigor tension
generation. Fish. Sci., 60: 717-721.
252 U. Erikson et al. /Aquaculture 149 (1997) 243-252
Norwegian Standard NS 4754, 198 1. Water analysis/alkalinity/potentiometric titration. (In Norwegian.)
Norwegian Standard NS 4734, 1988. Water analysis determination of dissolved oxygen-Titrimetric method.
(In Norwegian.)
Ostenfeld, T., Thomsen, S., Ing6lfdhttir, S., Ronsholdt, B. and McLean, E., 1995. Evaluation of the effect of
live haulage on metabolites and fillet texture of rainbow trout (Oncorhynchus mykiss). Water Sci.
Technol., 31: 233-237.
Reinert, R.E. and Hohreiter, D.W., 1984. Adenylate energy charge as a measure of stress in fish. In: V.W.
Cairns, P.V. Hodson and J.O. Nriagu (Editors), Contaminant Effects on Fisheries. John Wiley, New York,
pp. 151-161.
Robertson, L., Thomas, P. and Arnold, CR., 1988. Plasma cortisol and secondary stress responses of cultured
red drum (Sciaenops ocellatus) to several transportation procedures. Aquaculture, 68: 115- 130.
Schulte, P.M., Moyes, CD. and Hochachka, P.W., 1992. Integrating metabolic pathways in post-exercise
recovery of white muscle. J. Exp. Biol., 166: 181-195.
Sellevold, O.F.M., Jynge, P. and Aarstad, K., 1986. High performance liquid chromatography: a rapid isocratic
method for determination of creatine compounds and adenine nucleotides in myocardial tissue. J. Mol.
Cell. Cardiol., 18: 517-527.
Sigholt, T., Erikson, U., Rustad, T., Johansen, S., Nordtvedt and Seland, A., 1997. Handling stress and storage
temperature affect meat quality of farm-raised Atlantic salmon (Salvo salar). J. Food Sci. (in press).
Specker, J.L. and Schreck, C.B., 1980. Stress responses to transportation and fitness for marine survival in
