Meat Science 80 (2008) 1219

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Meat Science
journal homepage: www.elsevier.com/locate/meatsci

Review

Have we underestimated the impact of pre-slaughter stress on meat quality in ruminants?

D.M. Ferguson a,*, R.D. Warner b
a b

CSIRO Livestock Industries, FD McMaster Laboratories, Locked Bag 1, Armidale, NSW 2350, Australia Department of Primary Industries, Victoria, 600 Sneydes Road Werribee, VIC 3030, Australia

a r t i c l e

i n f o

a b s t r a c t
Stress is the inevitable consequence of the process of transferring animals from farm to slaughter. The effects of chronic stress on muscle glycogen depletion and the consequent dark cutting condition have been well documented. However, there has been little examination of the consequences of acute stress immediately pre-slaughter on ruminant meat quality. New evidence is emerging to show that non pHmediated effects on meat quality can occur through pre-slaughter stress in cattle and sheep. This paper reviews the general aspects of pre-slaughter stress in the pre-slaughter context. It then examines the impacts of pre-slaughter stressors on ruminant carcass and meat quality and considers remedial strategies for remediating and preventing pre-slaughter stress. Further quantication of the biological costs of pre-slaughter stress and the consequences to meat quality is required. Crown Copyright 2008 Published by Elsevier Ltd. All rights reserved.

Article history: Received 11 April 2008 Accepted 3 May 2008

Keywords: Cattle Meat quality Pre-slaughter stress Sheep Tenderness

Contents 1. 2. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . General response to pre-slaughter stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Fear . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Dehydration and hunger . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Physical activity and fatigue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. Physical injury . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Specific effects of pre-slaughter factors on meat quality traits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Lairage duration and conditions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Method of marketing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Pre-slaughter handling and animal management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. Transport . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Management and control of pre-slaughter stress. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Pre-slaughter supplements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1.1. Magnesium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1.2. Tryptophan . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1.3. Electrolytes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Appropriate livestock facilities and best practice animal handling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Selection for temperament . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 13 13 14 14 14 15 15 15 15 16 16 16 16 17 17 17 17 18 18

3.

4.

5.

1. Introduction All meat animals will experience some level of stress prior to slaughter and this in turn, may have detrimental effects to meat quality. The magnitude of any negative effect is generally thought

* Corresponding author. Tel.: +61 2 67761354; fax: +61 2 67761333. E-mail address: drewe.ferguson@csiro.au (D.M. Ferguson).

0309-1740/$ - see front matter Crown Copyright 2008 Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.meatsci.2008.05.004

D.M. Ferguson, R.D. Warner / Meat Science 80 (2008) 1219

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to be a function of the type, duration and intensity of the individual pre-slaughter stressors and the susceptibility of the animal to them (Ferguson et al., 2001). This has been the general view but the evidence underpinning it has been somewhat limited and indirect. There are notable exceptions here such as the reasonably wellunderstood stress-mediated losses in muscle glycogen that gives rise to the undesirable dark cutting condition (Tarrant, 1989). However, much less is known about the specic effects of individual pre-slaughter stressors and the interactions between them on biophysical changes in muscle and the consequential effects on meat quality traits. Furthermore, it is not entirely clear whether intra-animal variability in stress responsiveness can account for unexplained variance in sensory traits like tenderness. For example, Jacob, Pethick, and Chapman (2005) found that the average change in muscle glycogen in the semitendinosus and semimembranosus of sheep between farm and slaughter varied from negative to positive between consignments which was attributed to differences in stress responsiveness. The study of any pre-slaughter stressor requires good control and standardisation of the post-slaughter environment especially rigor temperature, which has profound effects it can have on key traits like tenderness and water-holding capacity (Bendall, 1973). With the implementation of eating quality assurance systems underpinned by critical control point methodology (eg Meat Standards Australia (MSA), Polkinghorne, 2006), standardisation of the post-slaughter environment has been achieved signicantly better than in the past. However, whilst good progress has been made, these models for predicting meat quality also enable us to estimate how much we do not know about the process. For example, (Warner, Ferguson, Cottrell, & Knee, 2007) concluded that the negative effects of acute pre-slaughter stress in beef cattle on eating quality, induced by the use of electric goads, could not be accounted for in the MSA model for predicting the eating quality of beef. Similarly, the model did not account for the variation observed between eight slaughter groups of cattle in consumer panel score and change in shear force in a study comparing different marketing methods by Ferguson, Warner, Walker, and Knee (2007) (see Fig. 1). Given this, there has been an increased emphasis on quantifying the impact of pre-slaughter stress and exploring strategies for mitigating any stress-mediated losses in meat yield and quality. The purpose of this paper is to review the current knowledge with regard to the impact of pre-slaughter stress on ruminant meat quality. 2. General response to pre-slaughter stress The pre-slaughter phase includes the conditions and practices that apply during the period when the animal is moved or mustered on-farm to entry into the knocking box or V-restrainer at the abattoir. During this period, animals can be exposed to a range of challenging stimuli including: (i) handling and increased human contact; (ii) transport; (iii) novel/unfamiliar environments; (iv) food and water deprivation; (v) changes in social structure (i.e. through separation and mixing), and (vi) changes in climatic conditions. These challenges perturb the animals homeostasis and an adaptive response is activated in an attempt to restore balance. This response can be non-specic and considerable variability exists between animals not only in their perception of the stressor but in their co-ordination of the response (Moberg, 2001). Both are modulated by several intrinsic animal factors (e.g. genetics, sex, age, and physiological state) and by past experiences and acquired learning (Boissy, 1995; Hemsworth & Barnett, 2001; Moberg, 2001). As a consequence of these pre-slaughter challenges, an animal may experience fear, dehydration and hunger, increased physical activity and fatigue and physical injury. Moreover, the inability to adequately resolve some of these states (e.g. dehydration or fatigue) may invoke further psychological distress.

2.1. Fear The activation and regulation of the neuroendocrinal response to fear-eliciting stimuli has been studied extensively (see reviews Chrousos, 1998; Moberg, 2001; Steckler, 2005). The two central integrated processes include the autonomic nervous system and hypothalamicpituitaryadrenal (HPA) axis. An autonomic response is typically initiated in reaction to acute stressors (e.g. human contact) that require a rapid response. Obvious physiological changes include tachycardia, increased respiration rate, elevated body temperature and redistribution of visceral blood volume towards skeletal muscle and the brain. Behavioural changes are also evident including heightened alertness, immobilisation, aggression and escape/avoidance. The sympatho-adrenal component of the autonomic response is mediated by catecholamines (epinephrine and norepinephrine). Activation of the HPA axis is manifested by the release of glucocorticoids (e.g. cortisol) from the adrenal cortex. It is also worth noting that the HPA axis operates independently of stressful situations in a circadian manner (Chrousos, 1998). Its baseline activity is essential for life. The secretion of catecholamines results in signicant changes in energy metabolism including lipolysis, glycogenolysis in muscle and gluconeogenesis (Kuchel, 1991). Furthermore, they have an anabolic effect on muscle protein metabolism through decreased protein degradation (Rooyackers & Nair, 1997). Increased secretion of glucocorticoids amplies the mobilisation of energy induced by the catecholamines (Dantzer, 1994) although the response is typically slower. They moderate the demand for glucose by some tissues whilst concomitantly stimulating hepatic gluconeogenesis to increase glucose delivery to skeletal muscle and the brain. The effect of glucocorticoids on muscle protein metabolism is less clear (Rooyackers & Nair, 1997). Sugden and Fuller (1991) reviewed several studies and concluded if there were effects on muscle protein degradation, these were likely to be transient and would only be elicited at particularly high pharmacological doses. In a recent study where sheep were given an ACTH challenge 6 h prior to slaughter that elicited a sustained elevation in blood cortisol concentration, there was no effect on shear force or change in shear force over ve days of ageing at 15 C (Ferguson, Lea, Niemeyer, & Daly, unpublished). Catecholamines, clearly invoke signicant changes in glucose metabolism. For example, the rate of glycogenolysis in response to epinenphrine injection is approximately 185 times higher than that observed during fasting (Tarrant, 1989). The glycogenolytic response to epinephrine will vary depending on muscle bre type (Tarrant, 1989) and the level of muscle activity will also affect this association between bre type and catecholamine induced glycogenolysis (Richter, Ruderman, Haralambos, Belur, & Galbo, 1982). Richter et al. (1982) showed that during high frequency stimulation of perfused rat muscle, the effect of epinephrine on glycogenolysis was very evident in slow twitch bres, whilst there was virtually no effect in the fast twitch bres. However, during lowfrequency stimulation, the exact opposite was found. Lacourt and Tarrant (1985) also showed that type I bres were more responsive to adrenaline injection in cattle. However, in response to the combination of physical activity and sympatho-adrenal activation associated with mixed penning of bulls, glycogen loss was higher in type II bres. Signicant depletion of muscle glycogen reserves pre-slaughter has a profound and well documented effect on several key meat quality attributes such as ultimate pH, tenderness and ageing potential, colour and water-holding capacity (see Gregory, 2003). The normal muscle glycogen concentration in cattle and sheep ranges between 75 and 120 mmol/kg (Immonen, Kauffman, Schaefer, & Puolanne, 2000; Lambert et al., 1998; Monin, 1981). Therefore, some losses can be accommodated before the concentration

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reaches a critical threshold of 4557 mmol/kg below which the normal ultimate pH in meat (5.55.6) will not be attained (Howard, 1963; Tarrant, 1989). Another relevant aspect of glycogen concentration apart from the direct association between glycogen concentration and ultimate pH in meat, is that it has also been shown to inuence post-mortem glycolytic rate in ovine muscle (Daly, Gardner, Ferguson, & Thompson, 2005; Ferguson, Daly, Gardner, & Tume, 2008). In these studies, a positive association was found between glycogen concentration and glycolytic rate adjusted to a constant temperature of 38 C. Whilst there is some evidence that muscle protein degradation is suppressed through the specic actions of catecholamines in particular, the direct consequences of this to meat tenderness and post-mortem proteolysis are not well characterised. There have only been a limited number of studies but the results suggest that the effects are not necessarily large. Sensky, Parr, Bardsley, and Buttery (1996) infused epinephrine into pigs for seven days prior to slaughter and reported transient and variable effects on the calpain enzyme system over an eight day post-mortem period. The effects on tenderness during ageing were not investigated. A single injection of epinephrine ve minutes before slaughter in lambs that had either been exercised or not exercised just prior to slaughter, had no effect on semimembranosus shear force at 1 or 3 days post-mortem (Bond, Can, & Warner, 2004). Warner, Ponnampalam, Suster, and Dunshea (unpublished) showed that an injection of epinephrine at 3 or 24 h pre-slaughter caused a reduction in MFI values in the Longissimus and semimembranosus, and the shear force values were also higher for group receiving epinephrine 24 h prior to slaughter. One of the difculties in quantifying the direct effects of catecholamines on proteolysis is the confounding associated effects on muscle pH through glycogen depletion. For example, high pHu is more conducive for calpain mediated proteolysis (Goll, Thompson, Li, Wei, & Cong, 2003). 2.2. Dehydration and hunger For most cattle and sheep that are directly consigned from farm to abattoir, the period of food and water deprivation is likely to be <24 h. However, there may be situations, where this period extends to 3648 h (e.g. slaughter stock purchased through saleyards). One of the most obvious impacts of food and water deprivation is weight loss. The trend is typically exponential whereby the rate of liveweight loss is fastest during the initial 12 h of food and water restriction and slower thereafter Shorthose and Wythes (1988). Typically in cattle, during the initial 2448 h of fasting, the majority of weight lost originates from excretion of gastrointestinal tract contents and urine. As the duration of food and water deprivation extends beyond 48 h, tissue catabolism and dehydration increase in their contribution to liveweight loss. Wythes and Shorthose (1984) concluded that carcass weight loss was typically not observed until after 24 h of food and water deprivation in cattle. In sheep, Thompson, OHalloran, McNeil, JacksonHope, and May (1987) reported that feed deprivation for 24, 48, 72 and 96 h resulted in a 3.5, 5.9, 7.3 and 7.9% loss in hot carcass weight, resepctively. With regard to food and water deprivation, it is the latter that is more critical from an animal welfare perspective given the risk of dehydration occurring. In general, animals have the opportunity to rehydrate after arrival at the abattoir as they typically have access to water whilst in lairage. Although it is recognised that even with access to water, not all animals will drink. Limited access to and unfamiliarity with watering facilities will contribute to the variability in drinking behaviour in novel environments. Failure to drink when water is available is a particular problem in young calves (Gregory, 2003) and lambs (Jacob, Pethick, Ponnampalam,

Speijers, & Hopkins, 2006). Jacob et al. (2006) measured urine specic gravity (SG) as an indicator of hydration status and observed that up to 50% of lambs slaughtered in two abattoirs over one year had urine SG values indicative of some dehydration. The physiological responses to food and water deprivation for periods up to 48 h in cattle and sheep generally indicate that ruminants can cope with these challenges. From ruminant food and water deprivation and/or transport research, measures of haemoconcentration (e.g. total protein, PCV, osmolality) were elevated following water deprivation indicating some level of dehydration in both cattle (Ferguson et al., 2008; Parker, Hamlin, Coleman, & Fitzpatrick, 2003; Phillips, Juniewicz, & Vontungeln, 1991) and sheep (Fisher et al., 2008; Parrott, Lloyd, & Goode, 1996). However, the level of dehydration would not be classed as being of clinical concern as many of the key measures were still within normal expected physiological ranges. 2.3. Physical activity and fatigue During the pre-slaughter phase, animals are subjected to additional physical demands. This arises through increased handling and movement and during transport particularly when the space allowance is insufcient to allow cattle and sheep to lie down during the journey. Additional energy is required to service these demands and this will have an impact on muscle glycogen concentration and potentially ultimate pH. However, it is the intensity of physical activity that is quite critical, as physical activity per se may not always result in glycogen depletion. For example, Lambert et al. (1998) demonstrated that fast-walking cattle at a speed of 8 km/h over 5 km did not affect glycogen concentration in the Longissimus. Increased activity, depending on the intensity and duration, will lead to changes in muscle metabolite concentration (e.g. creatine phosphate, glycogen), temperature and pH at slaughter (Warner, Bond, & Kerr, 2000; Warner et al., 2005). Furthermore, exercise stress has also been shown to affect sarcoplasmic reticulum (SR) function specically, calcium transport in several animal (Byrd, McCutcheon, Hodgson, & Gollnick, 1989; Luckin, Favero, & Klug, 1991; Ortenblad, Sjogaard, & Madsen, 2000) and human (Booth et al., 1997; Gollnick, Korge, Karpakka, & Saltin, 1991) studies. These results lend some support that SR function might be altered by pre-slaughter stress and this in turn may contribute to variations in post-mortem glycolysis and calpain mediated proteolysis. However, post-mortem SR functionality was not affected in one study where sheep were forced to run for 15 min prior to slaughter. The changes in both the rates of Ca2+ uptake and release in whole muscle homogenates were small and not signicant (Ferguson, 2003; Warner et al., 2005). In this investigation, the post-mortem glycolytic response to low voltage stimulation was signicantly lower in the muscles from exercised sheep but this was attributed primarily to the exercise mediated reduction in glycogen and increase in phosphate concentrations. The additional physical demands experienced by animals prior to slaughter may lead to fatigue but most animals have an opportunity to rest and recover in lairage prior to slaughter. 2.4. Physical injury It is generally recognised that the most prevalent physical injury that occurs during pre-slaughter handling is bruising. At slaughter, the excising of the bruised region on the carcass results in a net loss in carcass weight and yield. The key factors that have been linked to increased bruising have been reviewed by Gregory (2003). A survey of more then ten slaughter groups of cattle in Australia used histological ageing of bruises taken from beef carcasses

D.M. Ferguson, R.D. Warner / Meat Science 80 (2008) 1219

15
100

Shear force day 1-day 14 (N)

Shear force Panel MQ4 score

3. Specic effects of pre-slaughter factors on meat quality traits In the investigation of the impact of pre-slaughter factors (e.g. transport, marketing method) it needs to be recognised that some factors represent a combination of individual stressors such as those described above. These stressors will invoke different temporal response proles. For instance, the fear response to human contact during handling is immediate, acute and relatively short lived whereas the behavioural and physiological responses to water deprivation will not be evident until some time (1224 h) after the commencement of the deprivation period. Furthermore, as previously mentioned, the response proles can vary quite considerably between animals. These issues reinforce the importance of good experimental replication. Furthermore, it makes the task of isolating and characterising the underlying cause of a pre-slaughter factor-mediated change in meat quality all the more complex. The impacts of some of these factors were reviewed previously by Ferguson et al. (2001). 3.1. Lairage duration and conditions One of the important segments of the marketing chain where pre-slaughter stress can escalate is the period at the abattoir prior to slaughter. The area where livestock are held at the abattoir is often referred to as the lairage and it is the time in and conditions within lairage that are important with regard to pre-slaughter stress. In many European countries and in North America it is common to slaughter animals on the day of arrival whereas in Australia, New Zealand and other countries, animals are more typically slaughtered the day after arrival. In the latter countries, the lairage affords the animal an opportunity to rehydrate and rest and recover from transport. Therefore, it is quite important to ensure that the lairage facilities and conditions are conducive for this to occur. In a study where cattle behaviour in lairage was monitored overnight, Eldridge, Warner, Wineld, and Vowles (1989) reported that cattle situated near a noisy environment (next to unloading facilities) exhibited more movement than cattle held in pens in quieter locations. Although there were no differences in Longissimus ultimate pH between the two groups, the cattle from the noisy pens had higher carcass bruise scores. They concluded that in order to reduce stress and bruising, lairage yards should be lled and emptied in a manner which minimises movement past resting animals. The time spent in lairage tends to increase the incidence of dark cutting in beef cattle (Warner, Truscot, Eldridge, & Franz, 1998) and reduce the Longissimus glycogen concentration but there is little evidence for the duration of lairage having any inuence on eating quality or tenderness. Jacob et al. (2005) found no difference in consumer sensory scores for 5 day aged meat from lamb or mutton animals kept in lairage at the abattoir for 0, 1, or 2 days pre-slaughter. Similarly, Ferguson, Shaw, and Stark (2007) contrasted 3 h and 18 h lairage in feedlot cattle and observed no effect on shear force or compression values of unaged or 14 day aged Longissimus. 3.2. Method of marketing The major difference between direct consignment and saleyard or auction marketing is that cattle sold through saleyards are typically exposed to more handling and transport and longer delays between the farm and slaughter, and consequently, longer periods of time off feed before slaughter. There is also the increased likelihood of the mixing of unfamiliar mobs of cattle when saleyard marketing is used. Given this there is an increased risk for losses in meat quality but this has not always been observed. Warner et al., 1998 re-

80 60

60 40 40

20 20

0 1 2 3 4 5 6 7 8

Slaughter group
Fig. 1. Variation in consumer panel scores and the magnitude of reduction in shear force after 14 days ageing in eight groups of cattle slaughtered under similar conditions (Ferguson et al., 2007).

ported that cattle consigned directly to the abattoir had similar levels of dark cutting to those consigned via a saleyard in a large survey of 3850 beef carcasses. In contrast, Shorthose (1989) found a higher incidence of dark cutting in saleyard compared to directly consigned cattle. Under controlled experimental conditions, carcass bruising has been found to be higher in cattle undergoing saleyard marketing relative to the cattle consigned direct to the abattoir (Eldridge, Barnett, Warner, Vowles, & Wineld, 1986). Ferguson et al., 2007 showed that marketing of cattle via a saleyard resulted in a trend for reduced consumer acceptability of Longissimus steaks relative to cattle consigned directly to the abattoir. Out of the eight slaughter groups of cattle, marketing via a saleyard resulted in a signicant reduction in consumer acceptability of the Longissimus for two slaughter groups and a signicant increase in 1 day shear force values for four groups, relative to the directly consigned groups. A key feature of this study was the signicant variation between the slaughter groups irrespective of the marketing method (Fig. 1). These groups were very similar in terms of breed, nutritional background and age and were sourced from different farms within a 370 km radius of the abattoir. Furthermore, every effort was made to standardise the post-slaughter conditions which was evident by the similar rates in post-mortem muscle pH and temperature decline. 3.3. Pre-slaughter handling and animal management Due to food safety requirements, cattle and sheep are often washed in lairage to remove hide or eece contaminants such as excreta and dirt. The process of handling and washing the animals will elicit a sympatho-adrenal stress response and this in turn has been shown to have deleterious consequences to the incidence of dark cutting. Petersen (1983) showed that there was a linear relationship between the number of times sheep were washed preslaughter and the mean ultimate pH of the Longissimus. They did not observe any statistical association between the duration of the resting period after washing and ultimate pH. Subjecting lambs to a swim wash 3 h before slaughter increased the number of dark cutting carcasses which was accompanied by an increase in the toughness of the loin muscle (Geesink, Mareko, Morton, & Bickerstaffe, 2001). A toughening effect independent of ultimate pH was also observed in an earlier study where lambs were also swimwashed pre-slaughter (Bickerstaffe, Morton, Daly, & Keeley, 1996). Relative to the signicant body of literature of the negative effects of stress immediately prior to slaughter on pig meat quality (e.g. Channon, Payne, & Warner, 2000; Klont & Lambooy, 1995; Stoier, Aaslyng, Olsen, & Henckel, 2001; Warriss, Brown, Knowles, et al.,

Consumer panel MQ4 score (1-100)

to show that more then 50% of the bruises occurred after arrival at the abattoir (McCausland & Millar, 1982).

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Table 1 Effect of acute pre-slaughter stress (no prodder vs. electric prodder, 68 prods, 15 min pre-slaughter) on plasma lactate and meat quality measures (Warner et al., 2007) Trait Plasma lactate at slaughter (mmol/L) pH 1 h Temperature 1 h pHu Purge% (21 day) Shear force (2 day) (N) Shear force (21 day) (N) MSA CMQ4 consumer scorea No electric prodder 4.29 6.33 37.7 5.46 3.5 91.1 47.0 59.6 Electric prodder 7.12 6.29 37.7 5.38 5.4 89.2 51.0 55.6 Signicance P < 0.05 ns ns ns P < 0.05 ns ns P < 0.05

a CMQ4 score (1100) is a consumer weighted score based on assessments of tenderness, juiciness, avour and overall liking.

1995; Warriss, Brown, Nute, et al., 1995), there is a paucity of data in ruminants. (Warner et al., 2007) showed that acute stress induced by the application of electric goads to cattle 15 min pre-slaughter will detrimentally affect the water-holding capacity of the loin muscle and the consumer acceptability of 21 day aged loin (Table 1). No difference was found in muscle glycolytic rate, temperature decline and ultimate pH. They postulated that the reduction in the waterholding capacity of the muscle from stressed cattle was the causative factor in the reduction in consumer acceptability. Warner et al., 2005 reported that when lambs were subjected to acute exercise 15 min pre-slaughter it resulted in higher ultimate pH in the Longissimus and semimembranosus and more acceptable tenderness and juiciness in the longissmus. They previously found that acute exercise pre-slaughter in lambs caused a reduction in the water-holding capacity of the loin and leg muscles although there were no effects on the shear force values (Warner et al., 2000). Simmons et al. (1997) also showed that exercise immediately pre-slaughter had no inuence on meat tenderness in lambs. These results suggest that in ruminants, the direct impacts of stressful challenges in the immediate pre-slaughter period on tenderness are not consistent and this may be associated with the nature of the stressor. In a study examining a reduction in two pre-slaughter factors, notably transport duration and total time from feedlot to slaughter, Jeremiah, Newman, Tong, and Gibson (1988) showed that cattle undergoing minimal stress pre-slaughter (transported a short distance and slaughtered within 4 hrs of leaving feedlot) had more acceptable consumer panel scores for tenderness, avour and juiciness than their normal stress treatment group (mixed, trucked 160 km, and slaughtered up to 24 h after leaving the feedlot pen). As they did not measure the ultimate pH of the meat, it is not possible to determine if this was the cause for the change in consumer acceptability. 3.4. Transport The duration cattle and sheep are transported can be quite considerable (>18 h) particularly in countries like Australia. However, in the main, cattle and sheep destined for slaughter are not transported over long durations (<10 h). The stress response to road transport in livestock has received considerable research attention and the subject was reviewed by Knowles and Warriss (2000). The inuence of transport stress in cattle will vary depending on the type of animal and the conditions prevailing during the journey (see review by Tarrant, 1990). The results from cattle transport studies indicate that transport over moderate distances (<400 km) is unlikely to affect pHu (Eldridge & Wineld, 1988; Tarrant, 1989). However, when cattle are transported over much larger distances (e.g. 2000 km) or durations (e.g. 24 h), small increases of 0.10.2 pH units might occur (Tarrant,

1989; Wythes, Arthur, Thompson, Williams, & Bond, 1981). However, Knowles, Warriss, Brown, and Edwards (1999) only observed small reductions in glycogen concentration in four muscles in cattle transported 14, 21, 26, and 31 h. The magnitude of any effect on glycogen concentration, and therefore ultimate pH, will be governed by the condition of the cattle, their nutritional history and also the holding time in lairage. The on-board transport conditions can also be an important factor. Eldridge and Wineld (1988) examined the effects of different space allowances over moderate distances and whilst they did not observe any effect on pHu, the incidence of bruising was higher at the lowest (0.89 m2/animal) and highest (1.39 m2/animals) space allowances. In a latter study by Eldridge, Wineld, and Cahill (1988), reducing the space allowance/animal resulted in increased heart rate and movement scores over a moderate journey. The other important outcome of this study was that once cattle were habituated to transport, their heart rates were only 15% greater than those observed during grazing. This aligns with the general observation that loading and the initial stages of transport are the most stressful and after this initial period, animals adapt to the transport conditions (Pettiford et al., 2008; Warriss et al., 1995; Warriss et al., 1995).

4. Management and control of pre-slaughter stress 4.1. Pre-slaughter supplements Several pre-slaughter supplements have been developed and investigated for their efcacy to ameliorate the effects of preslaughter stressors. 4.1.1. Magnesium There has been considerable research interest in the role dietary magnesium supplementation could play in reducing the effects of pre-slaughter stress and improving meat quality (see review by Dunshea, DSouza, Pethick, Harper, & Warner, 2005). Magnesium has been shown to depress neuromuscular stimulation (Hubbard, 1973) and when fed in the diet it resulted in an attenuation of glucocorticoids and catecholamines secretion (Kietzmann & Jablonski, 1985). Most of this research has been undertaken in pigs and several studies have shown that dietary magnesium supplementation in pigs resulted in improved pork quality such as improved meat colour and reduced drip loss (e.g. Apple, Maxwell, deRodas, Watson, & Johnson, 2000; DSouza, Warner, Dunshea, & Leury, 1999; Otten, Berrer, Hartmann, Bergerhoff, & Eichinger, 1992). Moreover, dietary organic magnesium supplementation has been validated under commercial conditions as a viable method to improve meat quality in pigs (Hofmeyr, Dunshea, Walker, & DSouza, 1999). Magnesium supplementation (MgO) has also been shown to reduce the loss of glycogen from muscle in Merino lambs during the post-farm period leading up to slaughter (Gardner, Jacob, & Pethick, 2001). Lowe, Peachey, and Devine (2002) however, found no effect on muscle glycogen, ultimate pH or shear force values when lambs were fed magnesium as a bolus for 28 days prior to slaughter. Similarly, Apple, Watson, Coffey, Kegley, and Rakes (2000) fed magnesium in various forms to lambs for 95 days but found no effects on muscle colour although they did not measure glycogen or ultimate pH. DSouza, Warner, Leury, and Dunshea (2002) assert that in order for magnesium to have an effect on meat quality, the feeding should be short-term and no longer than 5 days, as the excess magnesium is excreted. 4.1.2. Tryptophan Tryptophan is the precursor for the important neurotransmitter serotonin. Serotonin is central to the regulation of a number of key

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biological functions including temperature regulation, arousal, pain sensitivity, feeding, sexual behavior, and aggression (Leathwood, 1987). As reviewed by Schaefer, Dubeski, Aalhus, & Tong, 2001, tryptophan supplements may moderate stress in animals by stimulating brain serotonin levels. In pigs, this effect was greatest after 5 days of supplementation during a 10 day feeding period (Adeola & Ball, 1992). However, no effect on ultimate pH, colour, or the incidence of PSE was observed. Henry, Seve, Mounier, and Ganier (1996) found an increase in brain serotonin levels and a decrease in the rate and extent of post-mortem pH decline in the Longissimus as a result of tryptophan supplementation over 28 days. Peeters, Driessen, and Geers (2006) reported that feeding tryptophan to pigs at 6 g/kg for 5 days had no effect on plasma cortisol or lactate at slaughter or on initial or nal post-mortem pH and muscle colour. In their second experiment, Peeters et al. 2006 showed that feeding tryptophan to pigs for 3 days reduced the aggression in response to mixing stress, in that high levels of dietary tryptophan decreased the total duration of ghting by approximately 50%. But they found no effects on meat quality and no difference in behaviour in response to several standard stress events. They concluded that although high levels of tryptophan may result in animals avoiding stressful situations, it had no effect on responses to unavoidable stressors that animals may experience prior to slaughter. The evidence would suggest that tryptophan supplementation does increase brain serotonin levels in pigs but the effects on attenuating the pre-slaughter stress response and associated changes to meat quality are somewhat inconclusive. 4.1.3. Electrolytes The pre-slaughter feeding of electrolytes to cattle has been shown to improve carcass yield but there were no effects on initial or nal pH, muscle colour or muscle water-holding capacity (Schaefer, Jones, Tong, & Young, 1990). Nutricharge, which is a commercially available electrolyte therapy, when fed to cattle, has been shown to increase carcass yield and reduce the incidence of dark cutting in cattle (Schaefer, Jones, & Stanley, 1997). In laboratory taste panel assessments, palatability attributes did not differ between electrolyte-treated bulls and untreated bulls; and an indication was obtained that the electrolyte supplementation, as formulated, may have produced detrimental effects on consumer acceptability (Jeremiah, Schaefer, & Gibson, 1992). The application of electrolyte solutions in livestock prior to and subsequent to transport are reported to maintain electrolyte balance and in doing so, potentially reduce dehydration and weight loss associated with transport (Schaefer et al., 1997). However, the value of providing electrolytes supplements compared with water only has been questioned (Parker et al., 2003). contrasted the effects of 0 h food and water deprivation (FWD), 60 hours FWD and 12 hours FWD followed by 48 h of transport in Bos indicus cattle. The transported cattle were able to maintain their blood acidbase within normal ranges. Moreover, plasma electrolyte concentrations were not different between the three treatments. They concluded that in view of this, the provision of electrolyte solutions rather than water alone was unlikely to be more effective in resolving the dehydration associated with long-term transport. Although they concluded that there may be limited benets of electrolytes per se over the provision of water alone, the advantage of electrolytes may relate to the enhanced palatability of the water, resulting in increased consumption before loading. This may be advantageous for cattle in unfamiliar yards and drinking systems to ensure adequate water intake before transport and reduce the chance of dehydration. However, there is anecdotal evidence that excessive drinking immediately prior to transport may be undesirable, as animals are more likely to lie down on the vehicle during the journey.

4.2. Appropriate livestock facilities and best practice animal handling One of the most effective means of minimising pre-slaughter stress is to ensure that the animal handling facilities enable smooth and efcient movement of livestock and that the stockpersons understand the principles of animal handling (Grandin, 2003). Whilst this message may seem obvious, there is a need to continue to reinforce it within the red meat industries. The costs to upgrade livestock facilities and some resistance to change handling practices are recognised as impediments to continued improvement. 4.3. Selection for temperament Temperament in livestock can be dened a number of ways but the preferred denition here is that it is the behavioural expression of the fearfulness of an animal in response to a challenging situation. Several behavioural tests, largely based on escape and/or avoidance behaviour, have been developed primarily for cattle (see review by Burrow, 1997). Selection for improved temperament or less fearful cattle, in particular, can facilitate both human (i.e. handler) and animal welfare benets. Animals that display less fearful behaviour during routine handling and management are less likely to injure themselves and their handlers. There is evidence to show that temperament is correlated with other physiological measures of stress (e.g. cortisol concentration) in both cattle (Fell, Colditz, Walker, & Watson, 1999; King et al., 2006) and sheep (Bickell, Boissy, Ferguson, & Blache, in preparation). This would suggest that selection for improved temperament will result in a general reduction in the magnitude of the stress response which in turn, may lead to reduced stress-mediated losses in meat quality. Unfortunately, the results from several cattle studies examining the association between temperament and meat quality traits have not been compelling. Intuitively, animals that display more obvious and vigorous escape/avoidance behaviour are more likely to incur bruising during pre-slaughter handling. However, the results from three separate studies (Burrow & Dillon, 1997; Fordyce, Goddard, Tyler, & Williams, 1985; Fordyce, Wythes, Shorthose, Underwood, & Shepherd, 1988) were inconclusive. Similarly, no association between temperament and the incidence of dark cutting or ultimate pH was observed in the studies by Fordyce et al. (1988) and Petherick, Holroyd, Doogan, and Venus (2002). In contrast, Voisinet, Grandin, OConnor, Tatum, and Deesing (1997) reported that temperament (subjective crush score) was signicantly correlated with the incidence of dark cutting as determined by subjective colour assessment in a study involving 306 cattle. Given that pH was not measured, the results need to be considered with some caution as colour may not be the most denitive measure of dark cutting. Another notable aspect of this study is that their sample comprised different groups of cattle that were mixed the night before slaughter. In contrast to the results of Voisinet, Grandin, OConnor, Tatum, and Deesing (1997), the results from several other workers suggest that the phenotypic association between temperament and tenderness or beef eating quality scores is either non-existent or very weak (Burrow, Shorthose, & Stark, 1999; Colditz et al., 2007; Kadel, Johnston, Burrow, Graser, & Ferguson, 2006; King et al., 2006; Petherick et al., 2002). Whilst the phenotypic relationship between temperament and tenderness appears tenuous, the same cannot be said for the genetic correlation (rg = 0.30.4) between these two traits in cattle (Kadel et al., 2006; Reverter et al., 2003). This important result indicates that selection for temperament based on the measurement of ight time will result in genetic improvement in tenderness.

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D.M. Ferguson, R.D. Warner / Meat Science 80 (2008) 1219 DSouza, D. N., Warner, R. D., Dunshea, F. R., & Leury, B. J. (1999). Comparison of different dietary magnesium supplements on pork quality. Meat Science, 51, 221225. DSouza, D. N., Warner, R. D., Leury, B. J., & Dunshea, F. R. (2002). Effect of dietary magnesium supplementation dose and duration on plasma magnesium levels in pigs. International Congress of Meat Science and Technology, Rome, Italy, 48, 582583. Dunshea, F. R., DSouza, D. N., Pethick, D. W., Harper, G. S., & Warner, R. D. (2005). Effects of dietary factors and other metabolic modiers on quality and nutritional value of meat. Meat Science, 71, 838. Eldridge, G. A., Barnett, J. L., Warner, R. D., Vowles, W. J., & Wineld, C. G. (1986). The handling and transport of slaughter cattle in relation to improving efciency, safety, meat quality and animal welfare. Melbourne, Australia: Department of Agriculture and Rural Affairs. Eldridge, G. A., Warner, R. D., Wineld, C. G., & Vowles, W. J. (1989). Pre-slaughter management and marketing systems for cattle in relation to improving meat yield, meat quality and animal welfare. Melbourne, Australia: Department of Agriculture and Rural Affairs. Eldridge, G. A., & Wineld, C. G. (1988). The behaviour and bruising of cattle during transport at different space allowances. Australian Journal of Experimental Agriculture, 28, 695698. Eldridge, G. A., Wineld, C. G., & Cahill, D. J. (1988). Responses of cattle to different space allowances, pen sizes and road conditions during transport. Australian Journal of Experimental Agriculture, 28, 155159. Fell, L. R., Colditz, I. G., Walker, K. H., & Watson, D. L. (1999). Associations between temperament, performance and immune function in cattle entering a commercial feedlot. Australian Journal of Experimental Agriculture, 39, 795802. Ferguson, D. M. (2003). Regulation of post-mortem glycolysis in ruminant muscle. PhD Thesis. University of New England, Armidale, Australia. Ferguson, D. M., Bruce, H. L., Thompson, J. M., Egan, A. F., Perry, D., & Shorthose, W. R. (2001). Factors affecting beef palatability Farmgate to chilled carcass. Australian Journal of Experimental Agriculture, 41, 879891. Ferguson, D. M., Daly, B. l., Gardner, G. E., & Tume, R. K. (2008). Effect of glycogen concentration and form on the response to electrical stimulation and rate of post-mortem glycolysis in ovine muscle. Meat Science, 78, 202210. Ferguson, D. M., Pettiford, S. G., Niemeyer, D. D. O., Lee, C., Paull, D. R., & Lea, J. M., et al. (2008). Effect of duration of road transport on cattle behavior and physiology. Journal of Animal Science, in preparation. Ferguson, D. M., Shaw, F. D., & Stark, J. L. (2007). Effect of reduced lairage duration on beef quality. Australian Journal of Experimental Agriculture, 47, 770773. Ferguson, D. M., Warner, R. D., Walker, P. J., & Knee, B. (2007). Effect of cattle marketing method on beef quality and palatability. Australian Journal of Experimental Agriculture, 47, 774781. Fisher, A. D., Niemeyer, D. D. O., Lea, J. M., Lee, C., Paull, D. R., & Reed, M. T. et al. (2008). The effects of 12, 30 or 48 hours of road transport on the physiological and behavioral responses of sheep. Journal of Animal Science, in preparation. Fordyce, G., Goddard, M. E., Tyler, R., & Williams, G. (1985). Temperament and bruising of Bos indicus cross cattle. Australian Journal of Experimental Agriculture, 25, 283288. Fordyce, G., Wythes, J. R., Shorthose, W. R., Underwood, D. W., & Shepherd, R. K. (1988). Cattle temperaments in extensive beef herds in northern Queensland. 2. Effect of temperament on carcass and meat quality. Australian Journal of Experimental Agriculture, 28, 689693. Gardner, G. E., Jacob, R. H., & Pethick, D. W. (2001). The effect of magnesium oxide supplementation on muscle glycogen metabolism before and after exercise and at slaughter in sheep. Australian Journal of Agricultural Research, 52, 723729. Geesink, G. H., Mareko, M. H. D., Morton, J. D., & Bickerstaffe, R. (2001). Effects of stress and high voltage electrical stimulation on tenderness of lamb m. Longissimus. Meat Science, 57, 265271. Gollnick, P. D., Korge, P., Karpakka, J., & Saltin, B. (1991). Elongation of skeletal muscle relaxation during exercise is linked to reduced calcium uptake by the sarcoplasmic reticulum in man. Acta Physiologica Scandinavica, 142, 135136. Goll, D. E., Thompson, V. F., Li, H., Wei, W., & Cong, J. (2003). The calpain system. Physiology Reviews, 83, 731801. Grandin, T. (2003). Solving livestock handling problems in slaughter plants. In Animal welfare and meat science (pp. 4268). Oxon, UK: CABI Publishing. Gregory, N. G. (2003). Animal welfare and meat science. USA: CABI Publishing (pp. 6492). Hemsworth, P. H., & Barnett, J. L. (2001). Humananimal interactions and animal stress. In G. P. Moberg & J. A. Mench (Eds.), The biology of animal stress Basic principles and implications for animal welfare (pp. 309336). Oxon, UK: CABI Publishing. Henry, Y., Seve, B., Mounier, A., & Ganier, P. (1996). Growth performance and brain neurotransmitters in pigs as affected by tryptophan, protein, and sex. Journal of Animal Science, 74, 27002710. Hofmeyr, C. D., Dunshea, F. R., Walker, P. J., & DSouza, D. N. (1999). Magnesium supplementation to reduce the incidence of soft, exudative pork under commercial conditions. In P. D. Cranwell (Ed.), Manipulating pig production VII (pp. 179182). Werribee, Australia: Australasian Pig Science Association. Howard, A. (1963). The relation between physiological stress and meat quality. In D. E. Tribe (Ed.), Carcass composition and appraisal of meat animals (pp. 1121). Melbourne, Australia: CSIRO. Hubbard, J. I. (1973). Microphysiology of vertebrate neuromuscular transmission. Physiology Reviews, 53, 674723. Immonen, K., Kauffman, R. G., Schaefer, D. M., & Puolanne, E. (2000). Glycogen concentrations in bovine longissimus dorsi muscle. Meat Science, 54, 163167.

5. Conclusions The aim of this review was to examine the current knowledge of the impact of pre-slaughter stress on ruminants and the consequential effect on meat quality. There is compelling evidence to demonstrate that pre-slaughter stress can have a signicant deleterious effect on meat quality traits in both beef and lamb. Furthermore, some of these effects have occurred independent of any stress-mediated change to ultimate pH. There is also a need to broaden the focus to traits other than pH and tenderness such as water-holding capacity and purge which are affected by acute pre-slaughter stress. In terms of ameliorating pre-slaughter stress the current prophylactic therapies lack consistency and efcacy. Whilst difcult to achieve because of economic and behavioural (human) issues, ongoing improvement in stock handling, handling facilities and stock management must be encouraged. We are of the view that the impact of pre-slaughter stress has been underestimated and that it is imperative that the issue receives more research attention. This needs to continue in the interests of optimising animal welfare and minimising losses in product yield and quality. References
Adeola, O., & Ball, R. O. (1992). Hypothalamic neurotransmitter concentrations and meat quality in stressed pigs offered excess dietary tryptophan and tyrosine. Journal of Animal Science, 70, 18881894. Apple, J. K., Maxwell, C. V., deRodas, B., Watson, H. B., & Johnson, Z. B. (2000). Effect of magnesium mica on performance and carcase quality of growingnishing swine. Journal of Animal Science, 78, 21352143. Apple, J. K., Watson, H. B., Coffey, K. P., Kegley, E. B., & Rakes, L. K. (2000). Comparison of different magnesium sources on lamb muscle quality. Meat Science, 55, 443449. Bendall, J. R. (1973). Postmortem changes in muscle. In G. H. Bourne (Ed.), The structure and function of muscle (pp. 243309). New York, US: Academic Press. Bickell, S. L., Boissy, A., Ferguson, D. M., & Blache, D. (in preparation). Sheep selected on their behavioural response to a social and human challenge differ also in their response to novelty. Physiology and Behaviour . Bickerstaffe, R., Morton, J. D., Daly, C. C., & Keeley, G. M. (1996). Interaction of preslaughter stress and low voltage electrical stimulation on muscle proteolytic enzymes and meat tenderness in lambs. In 42nd international congress of meat science and technology (pp. 420421). Lillehammer, Norway. Boissy, A. (1995). Fear and fearfulness in animals. Quarterly Review of Biology, 70, 165191. Bond, J. J., Can, L. A., & Warner, R. D. (2004). The effect of exercise stress, adrenaline injection and electrical stimulation on changes in quality attributes and proteins in semimembranosus muscle of lamb. Meat Science, 68, 469477. Booth, J., McKenna, M. J., Ruell, P. A., Gwinn, T. H., Davis, G. M., Thompson, M. W., et al. (1997). Impaired calcium pump function does not slow relaxation in human skeletal muscle after prolonged exercise. Journal of Applied Physiology, 83, 511521. Burrow, H. M. (1997). Measurements of temperament and their relationships with performance traits of beef cattle: A review. Animal Breeding Abstracts, 65, 477495. Burrow, H. M., & Dillon, R. D. (1997). Relationships between temperament and growth in a feedlot and commercial carcass traits of Bos indicus crossbreds. Australian Journal of Experimental Agriculture, 37, 407411. Burrow, H. M., Shorthose, W. R., & Stark, J. L. (1999). Relationships between temperament and carcass and meat quality attributes of tropical beef cattle. Proceedings of the Association for the Advancement of Animal Breeding and Genetics, 13, 227230. Byrd, S. K., McCutcheon, L. J., Hodgson, D. R., & Gollnick, P. D. (1989). Altered sarcoplasmic reticulum function after high-intensity exercise. Journal of Applied Physiology, 67, 20722077. Channon, H. A., Payne, A., & Warner, R. D. (2000). Halothane genotype, pre-slaughter handling and stunning method all inuence pork quality. Meat Science, 56, 291299. Chrousos, G. P. (1998). Stressors, stress and neuroendocrine integration of the adaptive response: The 1997 Hans Selye memorial lecture. In P. Csermely (Ed.), Stress of life from molecules to man (pp. 311335). New York, USA: Academy of Science. Colditz, I. G., Ferguson, D. M., Greenwood, P. L., Doogan, V. J., Petherick, J. C., & Kilgour, R. (2007). Regrouping unfamiliar animals in the weeks prior to slaughter has few effects on physiology and meat quality in Bos taurus feedlot steers. Australian Journal of Experimental Agriculture, 47, 763769. Daly, B. L., Gardner, G. E., Ferguson, D. M., & Thompson, J. M. (2005). The effect of time off feed prior to slaughter on muscle glycogen metabolism and rate of pH decline. Australian Journal of Agricultural Research, 57, 12291235. Dantzer, R. (1994). Animal welfare methodology and criteria. Revue Scientique et Technique de l Ofce International des Epizooties, 13, 291302.

D.M. Ferguson, R.D. Warner / Meat Science 80 (2008) 1219 Jacob, R. H., Pethick, D. W., & Chapman, H. M. (2005). Muscle glycogen concentrations in commercial consignments of Australian lamb measured on farm and post-slaughter after three different lairage periods. Australian Journal of Experimental Agriculture, 45, 543552. Jacob, R. H., Pethick, D. W., Ponnampalam, E., Speijers, J., & Hopkins, D. L. (2006). The hydration status of lambs after lairage at two Australian abattoirs. Australian Journal of Experimental Agriculture, 46, 909912. Jacob, R. H., Walker, P. J., Skerritt, J. W., Davidson, R. H., Hopkins, D. L., Thompson, J. M., et al. (2005). The effect of lairage time on consumer sensory scores of the M. Longissimus thoracis et lumborum from lambs and lactating ewes. Australian Journal of Experimental Agriculture, 45, 535542. Jeremiah, L. E., Newman, J. A., Tong, A. K. W., & Gibson, L. L. (1988). The effects of castration preslaughter stress and zeranol implants on beef: Part 1 The texture of loin steaks from bovine males. Meat Science, 22, 83101. Jeremiah, L. E., Schaefer, A. L., & Gibson, L. L. (1992). The effects of ante-mortem feed and water withdrawal, ante-mortem electrolyte supplementation, and postmortem electrical stimulation on the palatability and consumer acceptance of bull beef after ageing (6 days at 1 C). Meat Science, 32, 149160. Kadel, M. J., Johnston, D. J., Burrow, H. M., Graser, H., & Ferguson, D. M. (2006). Genetics of ight time and other measures of temperament and their value as selection criteria for improving meat quality traits in tropically adapted breeds of cattle. Australian Journal of Experimental Agriculture, 57, 10291035. Kietzmann, M., & Jablonski, H. (1985). On the blocking of stress by magnesiumaspartate hydrochloride in the pig. Praktische Tierarzt, 66, 328335. King, D. A., Pfeiffer, C. E., Randel, R. D., Welsh, T. H., Oliphint, R. A., Baird, B. E., et al. (2006). Inuence of animal temperament and stress responsiveness on the carcass quality and beef tenderness of feedlot cattle. Journal of Animal Science, 74, 546556. Klont, R. E., & Lambooy, E. (1995). Effects of preslaughter muscle exercise on muscle metabolism and meat quality studied in anesthetized pigs of different halothane genotypes. Journal of Animal Science, 73, 108117. Knowles, T. G., & Warriss, P. D. (2000). Stress physiology of animals during transport. In T. Grandin (Ed.), Livestock handling and transport (pp. 385407). Oxon, UK: Cabi Publishing. Knowles, T. G., Warriss, P. D., Brown, S. N., & Edwards, J. E. (1999). Effects on cattle of transportation by road for up to 31 hours. Veterinary Record, 145, 575582. Kuchel, O. (1991). Stress and catecholamines. In G. jasmin & M. Cantin (Eds.), Stress revisited 1. Neuroendocrinolgy of stress (pp. 80103). Basel, Switz: Karger. Lacourt, A., & Tarrant, P. V. (1985). Glycogen depletion patterns in myobres of cattle during stress. Meat Science, 15, 85100. Lambert, M. G., Knight, T. W., Cosgrove, G. P., Anderson, C. B., Death, A. F., & Fisher, A. D. (1998). Exercise effects on muscle glycogen concentration in beef cattle. New Zealand Society of Animal Production, 60, 243244. Leathwood, P. D. (1987). Tryptophan availability and serotonin synthesis. Proceeding of the Nutrition Society, 46, 143156. Lowe, T. E., Peachey, B. M., & Devine, C. E. (2002). The effect of nutritional supplements on growth rate, stress responsiveness, muscle glycogen and meat tenderness in pastoral lambs. Meat Science, 62, 391397. Luckin, K. A., Favero, T. G., & Klug, G. A. (1991). Prolonged exercise induces structural changes in SR Ca(2+)-ATPase of rat muscle. Biochemical Medicine and Metabolic Biology, 46, 391405. McCausland, I. P., & Millar, H. W. P. (1982). Time of occurence of bruises in slaughter cattle. Australian Veterinary Journal, 58, 253255. Moberg, G. P. (2001). Biological response to stress implications to animal welfare. In G. P. Moberg & J. A. Mench (Eds.), The biology of animal stress Basic principles and implications for animal welfare (pp. 122). Oxon, UK: CABI Publishing. Monin, G. (1981). Muscle metabolic type and the DFD condition. In D. E. Hood & P. V. Tarrant (Eds.), The problem of dark cutting in beef. Current topics in veterinary medicine and animal science (10, pp. 6381). The Hague, Netherlands: Martinus Nijhoff Publishers. Ortenblad, N., Sjogaard, G., & Madsen, K. (2000). Impaired sarcoplasmic reticulum Ca(2+) release rate after fatiguing stimulation in rat skeletal muscle. Journal of Applied Physiology, 89, 210217. Otten, W., Berrer, A., Hartmann, S., Bergerhoff, T., & Eichinger, H. M. (1992). Effects of magnesium fumarate supplementation on meat quality in pigs. In 38th international congress of meat science and technology (pp. 117). France: Clermont-Ferrand. Parker, A. J., Hamlin, G. P., Coleman, C. J., & Fitzpatrick, L. A. (2003). Quantitative analysis of acidbase balance in Bos indicus steers subjected to transportation of long duration. Journal of Animal Science, 81, 14341439. Parrott, R. F., Lloyd, D. M., & Goode, J. A. (1996). Stress hormone responses of sheep to food and water deprivation at high and low ambient temperatures. Animal Welfare, 5, 4556. Peeters, E., Driessen, B., & Geers, R. (2006). Inuence of supplemental magnesium, tryptophan, vitamin C, vitamin E, and herbs on stress responses and pork quality. Journal of Animal Science, 84, 18271838. Petersen, G. V. (1983). The effect of swimming lambs and subsequent resting periods on the ultimate pH of meat. Meat Science, 9, 237246. Petherick, J. C., Holroyd, R. G., Doogan, V. J., & Venus, B. K. (2002). Productivity, carcass and meat quality of lot-fed Bos indicus cross steers grouped according to temperament. Australian Journal of Experimental Agriculture, 42, 389 398. Pettiford, S. G., Ferguson, D. M., Lea, J. M., Lee, C., Paull, D. R., Reed, M. T., et al. (2008). The effect of loading practices and 6 hour road transport on the physiological responses of yearling cattle. Australian Journal of Experimental Agriculture, 48, 16.

19

Phillips, W. A., Juniewicz, P. E., & Vontungeln, D. L. (1991). The effect of fasting, transit plus fasting, and administration of adrenocorticotropic hormone on the source and amount of weight lost by feeder steers of different ages. Journal of Animal Science, 69, 23422348. Polkinghorne, R. J. (2006). Implementing a palatability assurance critical control point (PACCP) approach to satisfy consumer demands. Meat Science, 74, 180187. Reverter, A., Johnston, D. J., Ferguson, D. M., Perry, D., Goddard, M. E., Burrow, H. M., et al. (2003). Genetic and phenotypic characterisation of animal, carcass, and meat quality traits from temperate and tropically adapted beef breeds. 4. Correlations among animal, carcass, and meat quality traits. Australian Journal of Agricultural Research, 54, 149158. Richter, E. A., Ruderman, N. B., Haralambos, G., Belur, E. R., & Galbo, H. (1982). Muscle glycogenolysis during exercise: Dual control by epinephrine and contractions. American Journal of Physiology, 242, E25E32. Rooyackers, O. E., & Nair, K. S. (1997). Hormonal regulation of human muscle protein metabolism. Annual Reviews in Nutrition, 17, 457485. Schaefer, A. L., Dubeski, P. L., Aalhus, J. L., & Tong, A. K. W. (2001). Role of nutrition in reducing antemortem stress and meat quality aberrations. Journal of Animal Science, 79, E91E101. Schaefer, A. L., Jones, S. D., & Stanley, R. W. (1997). The use of electrolyte solutions for reducing transport stress. Journal of Animal Science, 75, 258265. Schaefer, A. L., Jones, S. D. M., Tong, A. K. W., & Young, B. A. (1990). Effects of transport and electrolyte supplementation on ion concentration, carcass yield and quality in bulls. Canadian Journal of Animal Science, 70, 107119. Sensky, P. L., Parr, T., Bardsley, R. G., & Buttery, P. J. (1996). Relationship between plasma epinephrine concentration and the activity of the calpain enzyme system in porcine Longissimus muscle. Journal of Animal Science, 74, 380387. Shorthose, W. R. (1989). Dark-cutting meat in beef and sheep carcasses under the different environments of Australia. In S. U. Fabiansson, W. R. Shorthose, & R. D. Warner (Eds.), Dark-cutting in Cattle and Sheep (pp. 6873). Sydney, Australia: Australian Meat and Livestock Research and Development Corporation. Shorthose, W. R., & Wythes, J. R. (1988). Transport of sheep and cattle. In Proceedings of the 34th international congress of meat science and technology (pp. 122129), Springer, Australia. Simmons, N. J., Young, O. A., Dobbie, P. M., Singh, K., Thompson, B. C., & Speck, P. A. (1997). Post-mortem calpain-system kinetics in lamb: Effects of clenbuterol and preslaughter exercise. Meat Science, 47, 135146. Steckler, T. (2005). The neuropsychology of stress. In T. Steckler, N. H. Kalin, & J. M. H. Reul (Eds.). Handbook of stress and the brain. Part 1: The neurobiology of stress (pp. 2542). London, UK: Elsevier Ltd.. Stoier, S., Aaslyng, M. D., Olsen, E. V., & Henckel, P. (2001). The effect of stress during lairage and stunning on muscle metabolism and drip loss in Danish pork. Meat Science, 59, 127131. Sugden, P. H., & Fuller, S. J. (1991). Regulation of protein turnover in skeletal and cardiac muscle. Biochemistry Journal, 273, 2137. Tarrant, P. V. (1989). Animal behaviour and environment in the dark-cutting condition. In S. U. Fabiansson, W. R. Shorthose, & R. D. Warner (Eds.), Darkcutting in cattle and sheep (pp. 818). Sydney, Australia: Australian Meat and Livestock Research and Development Corporation. Tarrant, P. V. (1990). Transportation of cattle by road. Applied Animal Behaviour Science, 28, 153170. Thompson, J., OHalloran, W., McNeil, L. D., Jackson-Hope, N., & May, T. (1987). The effect of fasting on liveweight and carcass characteristics in lambs. Meat Science, 20, 293309. Voisinet, B. D., Grandin, T., OConnor, S. F., Tatum, J. D., & Deesing, M. J. (1997). Bos indicus cross feedlot cattle with excitable temperaments have tougher meat and a higher incidence of borderline dark cutters. Meat Science, 46, 367377. Warner, R. D., Truscot, T. G., Eldridge, G. A., & Franz, P. R. (1998). A survey of the incidence of high pH beef meat in Victorian abattoirs. In 34th International Congress of Meat Science and Technology (pp. 150151). Brisbane, Australia. Warner, R. D., Ferguson, D. M., Cottrell, J. J., & Knee, B. (2007). Acute stress induced by the use of electric prodders pre-slaughter causes tougher beef meat. Australian Journal of Experimental Agriculture, 47, 782788. Warner, R. D., Bond, J. J., & Kerr, M. G. (2000). Meat quality traits in lamb M. Longissimus thoracis et lumborum: The effect of pre-slaughter stress and electrical stimulation. In 46th international congress of meat science and technology (pp. 154155). Argentina: Buenos Aires. Warner, R. D., Ferguson, D. M., McDonagh, M. B., Channon, H. A., Cottrell, J. J., & Dunshea, F. R. (2005). Acute exercise stress and electrical stimulation inuence the consumer perception of sheep meat eating quality and objective quality traits. Australian Journal of Experimental Agriculture, 45, 553560. Warriss, P. D., Brown, S. N., Knowles, T. G., Kestin, S. C., Edwards, J. E., Dolan, S. K., et al. (1995). Effects on cattle of transport by road for up to 15 hours. Veterinary Record, 136, 319323. Warriss, P. D., Brown, S. N., Nute, G. R., Knowles, T. G., Edwards, J. E., Perry, A. M., et al. (1995). Potential interactions between the effects of pre-slaughter stress and postmortem electrical-stimulation of the carcasses on meat quality in pigs. Meat Science, 41, 5568. Wythes, J. R., & Shorthose, W. R. (1984). Marketing cattle: Its effects on liveweight, carcases and meat quality. Australian Meat Research Corporation Review No. 46. Wythes, J. R., Arthur, R. J., Thompson, P. J. M., Williams, G. E., & Bond, J. H. (1981). Effects of transporting cows various distances on liveweight, carcase traits and muscle pH. Australian Journal of Experimental Agriculture and Animal Husbandry, 21, 557561.