Richard B. D'Eath

‘Freedom from hunger’ and preventing obesity: the animal welfare implications of reducing food quantity or quality

In animals, including humans, free access to high-quality (generally energy-dense) food can result in obesity, leading to physiological and health problems. Consequently, various captive animals, including laboratory and companion animals and certain farm animals, are often kept on a restricted diet. Quantitative restriction of food is associated with signs of hunger such as increases in feeding motivation, activity and redirected oral behaviours which may develop into stereotypies. An alternative approach to energy intake restriction is to provide more food, but of a reduced quality. Such alternative diets are usually high in fibre and have lower energy density. The benefits of these alternative diets for animals are controversial: some authors argue that they result in more normal feeding behaviour, promote satiety and so improve animal welfare; others argue that ‘metabolic hunger’ remains no matter how the restriction of energy intake and weight gain is achieved. We discuss the different arguments behind this controversy, focusing on two well-researched cases of food-restricted farmed livestock: pregnant sows and broiler breeders. Disagreement between experts results from differences in assumptions about what determines and controls feeding behaviour and food intake, from the methodology of assessing animal hunger and from the weighting placed on ‘naturalness’ of behaviour as a determinant of welfare. Problems with commonly used behavioural and physiological measures of hunger are discussed. Future research into animal feeding preferences, in particular the relative weight placed on food quantity and quality, would be valuable, alongside more fundamental research into the changes in feeding physiology associated with alternative diets.

Colour perception and the use of video playback experiments in animal behaviour

LEO J. FLEISHMAN*, WILLIAM J. McCLINTOCK†, RICHARD B. D’EATH‡, DAVID H. BRAINARD§ & JOHN A. ENDLER** *Department of Biological Sciences, Union College †Department of Ecology, Evolution and Marine Biology, University of California at Santa Barbara, U.S.A. ‡Animal Biology Division, Scottish Agricultural College, Edinburgh §Department of Psychology, University of California at Santa Barbara, U.S.A. **Department of Zoology and Tropical Ecology, James Cook University, Australia

Genetic validation of postmixing skin injuries in pigs as an indicator of aggressiveness and the relationship with injuries under more stable social conditions

The objective of the study was to estimate genetic correlations between skin lesions and aggressive behavior postmixing and under more stable social conditions as a potential means of selecting against pig aggressiveness. Postmixing aggression in commercial pig production is common, compromises welfare and profitability, and cannot be significantly reduced by low-cost changes to the environment. A genetic component to individual aggressiveness has been described in pigs and other species. Selective breeding against aggressiveness ought to be possible if an easily measured indicator trait can be shown to be genetically associated with aggressive behavior. Aggressive behavior was recorded continuously for 24 h after mixing, and a count of skin lesions (lesion count, LC) was recorded at 24 h and 3 wk postmixing on 1,663 pigs. Two behavioral traits were found to have a moderate to high heritability similar to that of growth traits; duration of involvement in reciprocal fighting (0.43 +/- 0.04) and delivery of nonreciprocal aggression (NRA; 0.31 +/- 0.04), whereas receipt of NRA had a lower heritability (0.08 +/- 0.03). Genetic correlations (r(g)) suggested that lesions to the anterior region of the body 24 h after mixing were associated with reciprocal fighting (r(g) = 0.67 +/- 0.04), receipt of NRA (r(g) = 0.70 +/- 0.11), and to a lesser extent, delivery of NRA (r(g) = 0.31 +/- 0.06). Lesions to the center and rear were primarily genetically associated with receipt of NRA (r(g) = 0.80 +/- 0.05, 0.79 +/- 0.05). Genetic correlations indicated that pigs that engaged in reciprocal fighting delivered NRA to other animals (r(g) = 0.84 +/- 0.04) but were less likely to receive NRA themselves (r(g) = -0.41 +/- 0.14). A genetic merit index using lesions to the anterior region as one trait and those to the center or rear or both as a second trait should allow selection against animals involved in reciprocal fighting and the delivery of NRA. Positive correlations between LC 24 h and 3 wk after mixing were found, especially for lesions to the center and rear of the body, indicating that postmixing lesions are predictive of those received under more stable group conditions. As well as reducing immediate aggression at mixing, selection on postmixing LC is expected to have a long-term impact on injuries from aggression, even after dominance relationships are established.

Environmental enrichment enhances spatial cognition in rats by reducing thigmotaxis (wall hugging) during testing

Rats, Rattus norvegicus, housed with ‘environmental enrichment’ do better in tests of spatial cognition than rats housed in barren cages. The leading hypothesis is that exposure to ‘social and inanimate complexity’ leads to better cognitive-processing abilities, which directly enhances performance in a spatial task. However, enrichment is associated with reduced stress responses and anxiety in novel or acutely stressful situations (cognitive tasks are typically both). Therefore, a plausible alternative hypothesis is that experience of enrichment indirectly enhances performance by reducing a rats anxiety levels during cognitive testing. We found that, irrespective of sex, enriched rats outperformed barren-housed rats in the Morris water maze. However, after accounting for the effects of thigmotaxis (a behavioural anxiety measure during testing), there was no significant difference in performance between enriched and barren-housed rats. Enriched rats were simply less thigmotactic and this indirectly improved their performance. This was true for both males and females. We conclude that enrichment reduces anxiety outside the home cage, in a cognitive test situation, and, subsequently, the cognitive benefits of enrichment occur because enriched animals are less anxious during cognitive testing.

Early life predictors of the development of aggressive behaviour in the domestic pig

Abstract Individuals show stable differences in their aggressive responses towards unfamiliar conspecifics. We investigated the extent to which variables present during early life could be identified that were correlated with these later individual differences in aggressive behaviour. The behaviour and growth of 125 domestic pigs, Sus scrofa , from 16 litters, were studied from birth until 18 days after weaning, when they were tested on two occasions in resident–intruder tests to measure their aggressiveness. Aggressiveness was affected by litter, although not by sex. A number of early life correlates of later resident–intruder aggressiveness were found at the litter level. Pigs became more aggressive if they had been born into larger litters. Pigs in these aggressive litters were more active in the 8-h period immediately after birth, perhaps taking longer to achieve satiety at the udder. They were also in poorer condition 2 days after birth. Aggressive pigs also engaged in more pushing with littermates over the whole preweaning period. The best correlates of aggressiveness appear to be a number of correlated variables relating to low nutrition, either prenatally or in the early postnatal period. The results are consistent with the concept that early environmental conditions can programme behavioural responses for later life.

The effect of confinement during lactation on the hypothalamic–pituitary–adrenal axis and behaviour of primiparous sows

Commercial sows are typically confined in crates before and during parturition and remain there throughout lactation. In various animal species including non-lactating pigs, confinement over similar periods leads to adaptive changes in the HPA axis, consistent with chronic stress. To investigate evidence for chronic stress in lactating sows, primiparous sows (gilts) were kept in behaviourally confining crates with straw bedding (CS, n = 8) or without bedding (C, n = 8) or in larger strawed pens (PS, n = 16) between 5 days before parturition until 29 days postpartum (piglets were weaned on day 28). Behavioural and physiological recordings (Plasma ACTH and cortisol) were taken at intervals (baseline), and CRH injections were given on five occasions (days 2, 8, 15, 22 and 29 postpartum). The PS gilts spent more time in substrate-directed behaviour and lying ventrally, and less time lying laterally and sitting than the two crated treatments (C and CS) throughout lactation. Baseline plasma ACTH and cortisol levels showed no treatment differences, although we confirmed that a diurnal pattern exists, with morning (1000 h) cortisol being higher than later in the day. CRH challenge tests suggested changes in the HPA axis, consistent with chronic stress, by the end of the lactation period. Cortisol response to CRH tended to be higher in CS than PS across all days, and by day 29 cortisol response to CRH was significantly higher in CS compared to PS and tended to be higher in C than PS. Cortisol/ACTH ratio following CRH challenge also tended to be higher in the crate treatments (C and CS) by day 29. These data suggest that prolonged confinement in farrowing crates may have a negative impact on sow welfare.

Resident–Intruder Trait Aggression is Associated with Differences in Lysine Vasopressin and Serotonin Receptor 1A (5‐HT1A) mRNA Expression in the Brain of Pre‐Pubertal Female Domestic Pigs (Sus scrofa)

Aggressive behaviour exhibited by domestic pigs following encounters with unfamiliar individuals is a serious welfare and economical problem. Aggression resulting in skin lesions is similarly prevalent in prepubertal pigs of either sex. Little is known about the neural circuits and neuropeptides that control aggression in the pig. Because there is evidence for the involvement of the vasopressin and serotonergic systems in the regulation of aggressive behaviour in male mammals, we sought differences using quantitative in situ hybridisation of vasopressin and serotonin 1A receptor (5‐HT1A) mRNA expression within specific brain regions of aggressive and nonaggressive prepubertal female pigs. The number of cells expressing vasopressin mRNA was significantly higher in aggressive pigs in the medial amygdala, lateral septum (LS) and showed a similar trend in the bed nucleus of the stria terminalis (BnST) but not the paraventricular nucleus (PVN) or supraoptic nucleus. The 5‐HT1A receptor was widely expressed through the porcine brain and a significantly lower intensity (silver grain density) of 5‐HT1A mRNA expression was observed in the BnST. In the medial amygdala and LS fewer cells expressed 5‐HT1A mRNA in aggressive pigs but no differences were found in the PVN. In the absence of inbred strains or selection lines, these findings have shown that prior identification of phenotypic behavioural extremes in a population in advance of neural studies is a useful technique. Moreover, these findings support a central role for vasopressin and serotonin in the mediation of high trait aggression in prepubertal female pigs.

Genetic associations between behavioral traits and direct-social effects of growth rate in pigs

This study examined the behavioral consequences of selecting pigs using a social genetic model for growth. Calculations enable each member of a group of pigs to be given a direct breeding value (DBV) and a social breeding value (SBV), which can be summarized into a total breeding value (TBV) for growth. Selection for growth TBV could affect animal behavior because social effects account for within-group interactions. Data were recorded from 96 groups of Yorkshire and Yorkshire × Landrace pigs in a nucleus herd. Each group contained 15 pigs fed ad libitum from 2 feeders; the space allowance was 0.85 m2/pig. Average daily gain was quantified from 35 to 100 kg of BW. Fighting and bullying activity at mixing (period 1), lying frequency 3 wk after mixing (period 2), and counts of skin lesions in periods 1 and 2 were recorded. The DBV for these traits were estimated with a classic animal model. We simulated different correlations between the direct genetic effect and the social genetic effect on growth rate (r(DS)), 2 components that respectively determine a pigs genetic capacity to grow and its genetic influence on growth of group mates: r(DS) was successively assumed to be 0 and ±0.12, ±0.20, ±0.29, and ±0.58. Finally, the correlations between DBV, SBV, and TBV for ADG, as well as the DBV for behavior and skin lesions, were calculated and tested for a level of significance at P < 0.05. The gradient from negative to positive values of r(DS) refers to a progressive path running from genetic antagonism to genetic mutualism for growth. If rDS in the population truly ranged between -0.58 and -0.20, correlations for TBV for ADG with DBV for fighting and bullying progressively increased with rDS. Consequently, if rDS was low (between -0.12 and +0.12) or positive (>+0.12), pigs with high TBV for ADG had higher DBV for bullying other pigs in the group and for fighting than pigs with lower TBV for ADG. Pigs with high TBV for ADG did not differ from other pigs in their DBV for lesions to the anterior part of the body, but they had a lower DBV for posterior lesions, whereas in period 2, they had higher DBV for posterior lesions and lower DBV for lying. Under genetic mutualism for growth and in housing conditions similar to those in the present study, selection for growth TBV would promote the rapid establishment of the dominance relationships, with more aggressive contests among group mates at mixing. Pigs would subsequently be more active but, judging by skin lesions, less willing to fight in a more stable social situation.

Sex differences, or not, in spatial cognition in albino rats: acute stress is the key

Male rats, Rattus norvegicus, typically outperform females in tests of spatial cognition. However, as stress affects cognition differently in the two sexes, performance differences may be an artefact of stress. Rats face at least two sources of stress during an experiment: the test situation (acute) and housing conditions (chronic, e.g. isolation). We used a task (the Morris water maze, MWM) that allowed testing of both spatial working and reference memory to investigate whether chronic stress (isolation housing) and/or acute stress (the task) has a differential impact on spatial cognition in male and female albino rats. Irrespective of age at the onset of isolation housing, isolated rats were not spatially impaired relative to pair-housed rats. However, the acute stress of the task led to adult males apparently outperforming adult females: adult females took longer to reach the platform than did males because they spent more time in thigmotaxis (swimming close to the wall) during testing. In juvenile rats, the stress caused by swimming in the MWM resulted in both males and females being highly thigmotactic and no sex difference in performance. We conclude that stress can lead to apparent differences between the sexes in performance on a spatial cognition task.

Sex differences in spatial cognition are not caused by isolation housing

Summary In mammals, males typically have better spatial ability than do females. However, most of the data come from laboratory tests and it is possible that factors impacting on the captive animal cause the observed sex differences in spatial cognition. A common influence on cognitive ability is stress, which may have its effect acutely, in the testing situation, or chronically, due to the housing conditions. We used a spatial working and reference memory task (the Morris water maze) to investigate if isolation housing had a differential impact on spatial cognition in male and female rats. Either as juveniles or as adults, rats were housed in pairs or in isolation. We also manipulated the duration of isolation housing. Regardless of housing condition, we found a sex difference in spatial ability only in the youngest rats. However, we found no evidence that isolated rats were spatially impaired relative to pair-housed rats. We also found no difference in body weight, food intake or bar biting behaviour (indicators of welfare in rodents) between pair and isolated rats. We conclude that isolation housing causes insufficient stress to cause sex differences in spatial cognition.