The effects of variations in the predictability of appetitive events, such as feeding, have rarely been studied in animals in general or primates in particular. Feeding animals on highly predictable temporal schedules often results in the performance of food anticipatory activity (FAA), characterised by increased arousal and activity and thought to be detrimental to welfare. Temporally unpredictable feeding schedules have been interpreted as resulting in improved welfare. However, if feeding is made unpredictable by preceding it with an unreliable signal, it may result in frustration and aggression. It is suggested here that two distinct but overlapping types of predictability exist. 'Temporal' predictability describes whether an event occurs at fixed or variable intervals, whereas 'signalled' predictability relates to the reliability of a signal preceding the event. This thesis examines the effects of each of these types of predictability in relation to feeding. Welfare was assessed in laboratory-housed common marmosets( Callithrix jacchus) using behavioural measures, which were identified in the context of the routine stressor of human handling and weighing. The signalled and temporal predictability of presentation of a desirable titbit was subsequently experimentally manipulated. It was found that temporally unpredictable presentation of food, preceded by an unreliable signal, was associated with substantially increased stress-related behaviours in this species. If no signal was used, stress increased to a moderate level, but if the food delivery followed a reliable signal there were few behavioural changes compared to control animals. Temporally predictable feeding, without a signal, was associated with lower rates of stress-related behaviour than temporally unpredictable, unsignalled feeding. However, deviations from this temporally predictable schedule, representing delays to feeding, resulted in marked increases in stress. The results were confirmed with a further study, worked around existing feeding routines and using a different primate species, the stump-tailed macaque (Macaca arctoides). Based on these findings it is suggested that the most beneficial schedule for feeding captive primates is a temporally unpredictable one, which appears to buffer animals against the negative effects of delays as well as minimising FAA. Presentation of a reliable signal before food delivery appears to minimise the stress intrinsically associated with a temporally unpredictable routine. These recommendations represent a simple and inexpensive method of improving the welfare of captive primates.

The common marmoset is the most frequently used New World primate in laboratory research and testing. In the UK, their use is strictly controlled by the Animals (Scientific Procedures) Act, which is underpinned by the principles of humane science: Replacement, Reduction and Refinement. Despite their use, there are a number of problems associated with the breeding of marmosets, including low dam longevity and increasing litter sizes. Large litters have led to high infant mortality and the need for human intervention to improve infant survival, which involves removal from the family for substantial periods of time. Previous research in a range of primate species shows that early life family separation is associated with numerous adverse behavioural and physiological effects. This project therefore sought to systematically investigate the effects of breeding and infant rearing practices, integrating a number of measures to assess the welfare of laboratory- housed marmosets. Potential predictors of dam longevity and litter size were first identified in three captive UK colonies, over four decades. Dam longevity was found to be approximately 6 years, with heavier dams living longer, but overall there was no consistent improvement in longevity over the decades. As longevity varied widely between colonies and over time, environment may be one of the most important factors. Approximately half of all births at each colony were litters larger than two, and these larger litters had greater infant mortality. Only dam weight at conception was useful in predicting litter size, with heavier dams producing larger litters. The consequences of large litters and early separation from the family for supplementary feeding were then investigated. Although twins had lower body weight than 2stays (two infants remaining with the family after death of the other littermate/s) and supplementary fed triplets, they also had the fewest health problems. There was also some evidence that animals from larger litters were more at risk of suffering from extreme low weight. Some minor differences were found in behavioural development between litter sizes. Singleton infants received more rejective rearing, while 2stays received more protective rearing, perhaps following the loss of an infant. While twin infants gained independence earlier than singletons or 2stays, they did not appear to cope better with stress in adulthood, displaying more significant increases in stress-related behaviour following the routine stressor of capture and weighing, compared to 2stays and supplementary fed triplets. While overall cortisol unexpectedly decreased from baseline to post capture, there were only significant fluctuations in 2stay marmosets. Instead, there were some increases in positive behaviour in supplementary fed triplets following the stressor, suggesting enhanced coping ability. However, in another group of supplementary fed triplets, there were subtle increases in depressive-like symptoms, measured using cognitive bias and preference tests, suggesting a reduced expectation of and interest in rewards. There were however no differences between family-reared and supplementary fed marmosets in time to learn a visual discrimination task, or in responses to temperament tests. Therefore, while it was hypothesised that early family separation would have adverse developmental consequences, there were actually very little differences between marmosets of different litter sizes and rearing backgrounds, across the range of measures. Results suggest that the current supplementary feeding programme, along with a regular human socialisation programme, minimises any potential negative effects. However, we should always be finding ways to improve the lives of animals in our care. Possible Refinements include reducing dam weight to increase twin births and improve infant survival, and training to allow supplementary feeding on the carrier’s back, to prevent infant separation and reduce disruption to the family. These Refinements could reduce fear and allow monkeys to become more resilient to the laboratory environment.

The social transmission of social behaviours in nonhuman primates has been understudied, experimentally, relative to instrumental, food-related behaviours. This is disproportional in relation to the comparatively high percentage of potential social traditions reported in wild primates. I report a systematic survey of the social learning literature and provide quantitative evidence of the discrepancy (Watson and Caldwell, 2009). Addressing the identified deficit in experimental work on social behaviours, I also report three empirical studies investigating the contagious nature of affective states in captive, socially housed marmosets. I carried out an observational study, to determine whether marmosets are influenced by spontaneously produced neighbour calls to perform a range of behaviours associated with similar affect. My results supported a neighbour effect for anxiety in marmosets. Consistent with previous findings for chimpanzees (Baker and Aureli, 1996; Videan et al., 2005), I also found evidence for neighbour effects for aggression and affiliation (Watson and Caldwell, 2010). Through experimental playback, I investigated contingent social contagion in the auditory and visual modalities. The playback of pre-recorded affiliative (chirp) calls was found to be associated with marmosets spending increased time in a range of affiliative behaviours. Playback of video showing conspecifics engaged in a positive affiliative behaviour (allogrooming) also appeared to cause marmosets to spend longer performing various affiliative behaviours. My results indicate that social contagion of affiliation is a multi-modal phenomenon in marmosets and also represent the first evidence that allogrooming is visually contagious in primates. Sapolsky (2006) conceptualised culture as the performance of species-typical behaviours to an unusual extent, termed ‘social culture’. Researchers have yet to directly investigate a transmission mechanism. I investigated whether a social culture of increased affiliation could be initiated in marmosets through the long-term playback, of positive calls, or of video of positive behaviour. The results were consistent with a relatively long-lasting influence of the playback of affiliative calls across several affiliative behaviours. The effect appeared to last substantially beyond the specific hours of playback, between playbacks, and after playback had ceased, potentially indicating a temporary shift in social culture. These results are preliminary but provide some support for the proposal that auditory social contagion may be a transmission mechanism for social culture. The long-term video playback of allogrooming appeared to result in a transitory shift in performance of the identical behaviour (increased allogrooming) after playbacks had ceased. In addition to theoretical implications for social cognition and social culture, my findings have potential practical application for the enhancement of welfare in captive marmosets through sensory, and non-contact social, enrichment.

There are numerous guidelines recommending that captive primates live in complex environments in which they have the opportunity to make choices and the ability to control aspects of the environment, despite the lack of quantitative evidence to suggest these qualities improve welfare. Complexity, choice and control (the ‘Three Cs’) are inter-related and therefore it is complicated to separate their effects. The main aim of this thesis was to examine how the ‘Three Cs’ affect welfare, using the common marmoset (Callithrix jacchus) as a model. Behavioural measures and preference tests were used to determine the impact and significance of the ‘Three Cs’ on welfare. Experimental manipulations were natural (i.e. access to outside runs), or unnatural (e.g. pressing a button to control additional illumination). In a series of different studies, marmosets were moved to larger and more complex enclosures, were allowed to choose between indoor cages and outdoor complex enclosures and were able to control additional white light or coloured lights in their home enclosures. The results of these studies show that appropriate levels of each of the ‘Three Cs’ had a positive influence on the welfare of the marmosets, especially on youngsters. Although having control over light, and increased illumination itself improved welfare, providing a choice of access to outside runs (which were more complex and allowed the marmosets greater control over their activities) resulted in the greatest welfare improvement for marmosets of all ages. Loss of access, or control, did not appear to have a negative impact. The marmosets were housed in pairs or in family groups, in the different studies. A cross-study comparison shows that the composition of the groups affected the behavioural response of adult marmosets to environmental enrichment. Unexpectedly, it was also found that, when housed in standard laboratory conditions, adult marmosets were more relaxed when housed in pairs than when housed with their offspring. A secondary aim of the thesis was to quantify welfare indicators and activity budgets of common marmosets in a range of different social and physical contexts, and to compare this with the behaviour of wild marmosets, to increase our understanding of what is “normal” in captive situations. It is concluded that it is critical to sub-divide locomotion and inactivity into different levels to interpret these measures accurately. Levels of calm locomotion increased in enriched environments, while levels of relaxed inactivity and scent marking decreased. A number of recommendations for the care and housing of marmosets are made.

Indiana University-Purdue University Indianapolis (IUPUI) / Seven human alcohol dehydrogenase genes (which encode the primary enzymes involved in alcohol metabolism) are grouped into classes based on function and sequence identity. While the Class I ADH isoenzymes contribute significantly to ethanol metabolism in the liver, Class IV ADH isoenzymes are involved in the first-pass metabolism of ethanol. It has been suggested that the ability to efficiently oxidize ethanol occurred late in primate evolution. Kinetic data obtained from the Class I ADH isoenzymes of marmoset and brown lemur, in addition to data from resurrected ancestral human Class IV ADH isoenzymes, supports this proposal--suggesting that two major events which occurred during primate evolution resulted in major adaptations toward ethanol metabolism. First, while human Class IV ADH first appeared 520 million years ago, a major adaptation to ethanol occurred very recently (approximately 15 million years ago); which was caused by a single amino acid change (A294V). This change increases the catalytic efficiency of the human Class IV enzymes toward ethanol by over 79-fold. Secondly, the Class I ADH form developed 80 million years ago--when angiosperms first began to produce fleshy fruits whose sugars are fermented to ethanol by yeasts. This was followed by the duplication and divergence of distinct Class I ADH isoforms--which occurred during mammalian radiation. This duplication event was followed by a second duplication/divergence event which occurred around or just before the emergence of prosimians (some 40 million years ago). We examined the multiple Class I isoforms from species with distinct dietary preferences (lemur and marmoset) in an effort to correlate diets rich in fermentable fruits with increased catalytic capacity toward ethanol oxidation. Our kinetic data support this hypothesis in that the species with a high content of fermentable fruit in its diet possess greater catalytic capacity toward ethanol.