The attitudes of experts towards the husbandry of captive Great Apes was sought in order to gain a greater understanding of the potential importance of different features of the captive environment that may be critical in maintaining a high standard of welfare. Following initial consultation with the convener of the Primate Taxon Advisory Group of the Australasian Regional Association of Zoological Parks and Aquaria, 17 husbandry attributes, such as social structure of the group, enclosure size and staff qualifications, each with two to four levels (ie husbandry scenarios) of possible provision in an enclosure were identified and described. An online survey using Adaptive Conjoint Analysis was distributed internationally to relevant stakeholders: zoo management staff, keepers and education staff, research colony personnel, veterinarians, animal welfare organisation representatives and scientists. A total of 359 respondents completed the survey, and the average importance values for the attributes, and rank order of importance for each of their levels were calculated. Great Ape social structure, enclosure appearance, group size, avoidance provision and enclosure furnishings were considered the most important attributes of captive Great Ape husbandry, whereas feeding interval, staff qualifications, the inclusion of plants within the enclosure, enrichment rotation, and the amount of time an animal spent in an outdoor enclosure were considered of low importance. The order in which these issues were ranked was influenced by the Great Ape species, with physical attributes of the enclosure being rated as more important for orangutans (Pongo pygmaeus) and group social attributes more important for the other species. Stakeholder group had little influence on the ranking of issues. It is concluded that experts provided a consensus view on the importance of husbandry attributes of the different Great Ape species that can be used to evaluate their welfare.

Human interaction as environmental enrichment for chimpanzees (Pan troglodytes) and other primates is widely promoted and believed to be of value, but has been subject to little objective evaluation. This study assessed the effects of positive human interaction (eg relaxed treat feeding, playing, and other forms of social interaction compatible with personnel safety) on the behaviour of adult chimpanzees. Subjects were housed indoors in groups of two or three individuals. The level of interaction during routine care and management (ie in the process of cleaning, feeding, and monitoring) represented the baseline condition. The test condition involved a familiar caretaker spending an additional 10 mins per day, 5 days a week, with each chimpanzee. This study was designed to assess carry-over effects of interaction on behaviour outside the context of care staff presence. Therefore, in all phases of the study, data (97 h of focal animal sampling) were collected only when caretakers were absent from the building. During the increased human interaction phase, the chimpanzees groomed each other more and showed lower levels of the following behaviours: regurgitation/reingestion, other oral abnormal behaviours, inactivity, and reactivity to the displays of neighbouring groups. A trend towards reduced agonistic display was also detected. Attempted interactions with the observer shifted significantly from predominantly aggressive to predominantly affiliative in nature. These results suggest that simple, unstructured affiliation between humans and chimpanzees should be a valued component of behavioural management.

There is an ethical and scientific need to minimise the harm experienced by animals used in scientific procedures and to maximise their well-being. Welfare can be improved by the refinement of practice, particularly if these refinements are applied to every aspect of the life of an animal used in the laboratory, from birth to death. Primates are considered likely to have a greater capacity for suffering than other sentient species and therefore refinement of their use is particularly important. The refinement of the human impact on laboratory-housed primates and of housing and husbandry practices are dealt with in parts I and II of this three-part review. In part III, methods of refinement that can be applied specifically to the use of primates in procedures, are summarised and discussed, together with a description of some current practices, and the scientific evidence that suggests that they should no longer be used. Methods of refinement of identification, capture and restraint, sampling, administration of substances, humane endpoints, and euthanasia are included. If these methods are used, taking into account species-specific differences and needs, it is concluded that harm can be minimised and primate welfare improved.

Members of the New World primate genera Callithrix and Cebuella have specialisations for eating plant exudates. Exudates are also an important component of the diets of many other callitrichid species in the wild, especially at times of nutritional stress. Gum arabic is fed daily to all marmosets and to some tamarins in Jersey Zoo's collection. This study investigated species differences in liking for gum and the effects of the concentration of gum solutions on palatability. As predicted from field data, Callithrix species consumed more gum than other species; Saguinus also showed quite a strong liking for gum. In parallel with data from the wild, lion tamarins (Leontopithecus spp.) consumed the least, and Callimico also took relatively little. The two marmoset species tended to like stronger solutions of gum more than weak solutions and, therefore, the provision of smaller amounts of stronger concentrations is likely to be the most cost-effective way of incorporating gum into the diet. Providing gum to callitrichids on a regular basis can have significant welfare benefits.

Bodyweight is an important health and welfare indicator for captive non-human primates (NHPs). Bodyweight can be measured during routine handling procedures, which cause stress. Alternatively, animals can be trained to step onto a scale, but training success varies greatly between individuals. Being able to weigh animals regularly without having to handle or train them is thus desirable for monitoring animal health and welfare. This study investigates the utility, ie the participation, reliability and time investment, of voluntary weighing in captive NHPs living in large social groups. Subjects of the study were 92 rhesus macaques (Macaca mulatta) housed in four social groups at the Biomedical Primate Research Centre in Rijswijk, The Netherlands. A scale was placed in their home enclosure during several sessions. Individuals were unwilling to step onto an unbaited scale. When likeable food items were used to attract individuals to the scale, 68% of them stepped onto the scale. Age and dominance rank did not affect stepping onto the scale, whereas exploratory tendency and social group did. The level of agreement between bodyweight by voluntary weighing and bodyweight measured during sedation was very high. These results show that the majority of rhesus macaques in social groups can be weighed voluntarily and that voluntary weighing is reliable. When optimising and further developing the method, voluntary weighing can form a valuable tool in the captive management of NHPs.

In Callitrichid primates, offspring remain in their natal group beyond the age of sexual maturity, increasing the group's inclusive fitness by cooperatively rearing their siblings. Contraception of the dominant female in these groups may alter the associated costs and benefits of this cooperative rearing in such a way that offspring themselves attempt to breed when a period longer than the normal inter-birth interval of one year has elapsed. Contraception of the dominant female may also induce changes in socio-sexual interactions between group members, which can lead to increased aggression after a short period. In this study, we investigated the occurrence of aggression in 16 captive groups of golden-headed lion tamarins (Leontopithecus chrysomelas) under three conditions: 1) no contraception used; 2) contraception used and offspring younger than one year present within the group; and 3) contraception used and all offspring in the group older than one year. We found that the probability of aggression occurring in the groups was best predicted by logistic regression models containing the factors ‘group size ‘ and ‘overall proportion of males ‘ or ‘number of sons ‘. Aggression was more likely in larger groups with a high proportion of males or a large number of sons. This effect was significantly stronger for groups in which all offspring were older than one year. Absence of dispersal opportunities and differences in male and female reproductive strategies may explain the observed patterns. The increased instability of large non-breeding groups presents a problem when using long-term contraceptive methods and should be taken into account when making decisions on the most suitable population-control procedures.

Finding a responsible method of population control that does not compromise animal welfare is a pressing problem for zoological institutions and conservation breeding programmes. This is exemplified by the conservation breeding programme of the golden-headed lion tamarin, Leontopithecus chrysomelas. The number of golden-headed lion tamarins in captivity is currently being limited by, among other means, the use of contraception. We have conducted a study on the effects of contraceptive methods used in golden-headed lion tamarins. Data were collected through the distribution of a survey. The use of Melengestrol acetate (MGA) implants in females was by far the most widespread contraceptive method. It was very effective in preventing reproduction, provided that females were not pregnant at the time of implantation. Pregnancies that had commenced before MGA implantation were carried to term and resulted in viable infants, as far as noted. However, the degree of reversibility was very low and, if females did conceive after MGA implantation, infant survival was lower than expected. The widespread use of MGA implants in golden-headed lion tamarins (and probably other species) should be seriously reconsidered. Alternative methods of population control should be investigated. Possible options include the use of other contraceptive methods, limiting the number of offspring through natural factors and the use of euthanasia under very strict conditions. Animal welfare implications associated with the use of euthanasia are discussed.

There is a growing awareness that non-human primates kept in zoos and laboratories deserve more species-appropriate stimulation because of their biological adaptation to a challenging environment.

Numerous attempts have been made to effectively emulate the gathering and processing aspects of natural feeding. Whole natural food-items, woodchips mixed with seeds, the puzzle ceiling and the puzzle feeder stocked with ordinary biscuits, cost little or nothing but induce sustained food gathering and/or food processing. Turf and fleece substrates sprinkled with particles of flavoured food, foraging trays, probe feeders and puzzles baited with food treats also promote more foraging behaviour, but they are relatively expensive and require added labour time to load and clean them.

Modern zoos are increasingly successful in maintaining and breeding exotic species. Many of the animals bred in captivity cannot be housed in their natal zoo nor in other recognized zoos in the region. These ‘surplus ‘ animals create a problem as zoos only have limited space at their disposal. The options open in this situation are to avoid the problem by preventing the animals from breeding (sterilization or contraception) or to dispose of the surplus animals (euthanasia; or transfer either to institutions not recognized by any national zoo federation or to a zoo outside the region, possibly using the services of an animal dealer). The pros and cons of all these options are evaluated in terms of practicality, welfare and ethics. In many cases, the judicious use of a combination of contraception and euthanasia would seem the most acceptable choice from an animal welfare point of view. Nevertheless, it is believed that considerably more research is needed into the methods and welfare aspects of contraception and sterilization.

The influence of an environmental enrichment feeding device (puzzle feeder), on activity and behaviour patterns of captive orang-utans, gorillas and chimpanzees was studied at London Zoo. General activity levels and behaviours directed towards the feeder increased for all species when the feeder was filled with food Chimpanzees used the feeder significantly more (18% of observation periods) than either gorillas (10%) or orang-utans (9.4%). There was considerable individual variation of puzzle use by individuals within each group and time of day also affected use. In some instances abnormal behaviours were reduced. These results are discussed in relation to the management of captive great apes and it is suggested that the use of puzzle feeders can improve the welfare of these animals.

In modern zoos, training should be an integral component of the animal care and management. The benefits of training include the opportunity for positive interactions with caretakers. This study was carried out with a group of vervet monkeys (Chlorocebus aethiops) housed at the Garda Zoological Park, Italy. Using focal animal sampling, we observed the behaviour performed by all group members from December 2007 to August 2008. The group took part in a training programme to be isolated in a familiar area before the subjects were included in a cognitive study. We collected behavioural data during a pre-training period to assess the social behaviour of the colony and during the training period to investigate the effects of the training programme on the behaviour of individuals. Additionally, a second phase of the study was conducted and training sessions with individual monkeys were video-recorded to determine the behaviour of animals during each training session and to thus confirm that they were suitable for participating in the procedure. Our results suggest that the training programme enriched the daily routine of these captive primates by increasing affiliative behaviours while decreasing agonistic behaviours. Furthermore, there was behavioural response variability among the individuals under the training procedure. However, all the individuals were trained to calmly enter a familiar area and be isolated from other members of the group. In conclusion, our findings highlight the importance of using positive reinforcement training to reduce the tension directly associated with potentially stressful procedures by allowing primates to participate voluntarily in these procedures. In addition, the training was found to be an enrichment tool for vervet monkeys.

Researchers searching for alternatives to painful procedures that involve animals may find that the dispersed relevant literature and the array of databases make the search challenging and even onerous. This paper addresses a significant gap that exists for researchers, in identifying appropriate databases to use when searching for specific types of information on alternatives. To facilitate the efficient and effective searching by users, and to ensure compliance with new requirements and improved science, we initiate an evolving guide comprising search grids of database resources organised by animal models and topics (http://www.vetmed.ucdavis.edu/Animal_Alternatives/databaseapproach.html). The search grids present organised lists of specific databases and other resources for each animal model and topic, with live links. The search grids also indicate resources that are freely available worldwide, and those that are proprietary and available only to subscribers. The search grids are divided into two categories: ‘animal models’ and ‘topics’. The category ‘animal models’ comprises: animal model selections; mice; rodents — rats/guinea pigs/hamsters; rabbits; dogs, cats; farm animals, sheep, swine; non-human primates; fish, frogs, aquatic; and exotics. The category ‘topics’ comprises: husbandry; behaviour; euthanasia; toxicity; monoclonal antibodies; teaching; endpoints; disease models; analgesia/anaesthesia; emerging technologies; strategies for specific intervention procedures; and standard operating procedures (for example, drawing blood, behavioural training, transportation, handling, restraint and identification). Users are provided with a selected list of linked resources relevant to their particular search. Starting with an appropriate database that covers the type of information that is being sought is the first step in conducting an effective search that can yield useful information to enhance animal welfare.

A technique measuring leukocyte (neutrophil) activity was used to examine differences between stress levels in a breeding colony of rhesus macaques housed in either a traditional caging system or open-rooms. The leukocyte activation test measured the degree to which blood from the two treatment groups could launch a further neutrophil response (superoxide production) to an in vitro challenge. Animals housed in a traditional caging system produced a significantly lower leukocyte response than animals housed in open-rooms, indicating that there was a higher level of stress associated with caged housing than open-room housing. This was not influenced by whether animals were physically restrained or trained to stand for a sedating injection. No differences were found between treatment groups in leukocyte numbers or composition. This study validates the use of the leukocyte activation test to assess physiological stress levels in non-human primates and demonstrates the animal welfare benefits of open-room housing over traditional laboratory caging systems.

Positive reinforcement training is one component of behavioural management employed to improve psychological well-being. There has been regulatory promotion to compensate for restricted social housing in part by providing human interaction to singly caged primates, implying an efficacy standard for evaluating human interaction. The effect of positive reinforcement training on the behaviour of 61 singly housed laboratory rhesus macaques (Macaca mulatta) was evaluated at two large primate facilities. Training involved body part presentation and basic control behaviours. Baseline data were compared to two treatment phases presented in varying order across individuals, six minutes per week of positive reinforcement training and six minutes per week of unstructured human interaction. While a MANOVA involving behavioural categories and study conditions across study subjects was significant, univariate ANOVAs found no effect of phase within any behavioural category. Categorising subjects according to rearing, housing facility, or baseline levels of abnormal behaviour did not reveal changes in behaviour with positive reinforcement training or human interaction. This study failed to detect, to any degree, the types of behavioural changes documented in the scientific literature to result from pairing singly housed monkeys. Implementing short durations of positive reinforcement training across large numbers of singly housed animals may not be the most effective manner for incorporating positive reinforcement training in the behavioural management of laboratory macaques. Rather, directing efforts toward individuals with specific behavioural, management, clinical, research or therapeutic needs may represent a more fruitful approach to improving psychological well-being with this technique.

A review of the scientific literature gives evidence that transferring previously single-caged adult macaques to permanent compatible pair-housing arrangements (isosexual pairs, adult/infant pairs) is associated with less risk of injury and morbidity than transferring them to permanent group-housing arrangements. Juvenile animals can readily be transferred to permanent group-housing situations without undue risks. Safe pair formation and subsequent pair-housing techniques have been developed for female and male rhesus (Macaca mulatta), stump-tailed (M. arctoides) and pig-tailed macaques (M. nemestrina) as well as for female long-tailed macaques (M. fascicularis). Pair housing does not jeopardize the animals’ physical health but it increases their behavioural health by providing them with an adequate environment to satisfy their need for social contact and social interaction.

Laboratory primates are often housed in same-sex pairs to avoid single-housing and when breeding is to be prevented. However, pair formation is not without risks, as fights and injuries may occur. No data are available on pair formation in female common marmosets (Callithrix jacchus), a species used extensively in laboratories. Therefore, this study focuses on the pairing of unfamiliar common marmoset females, aiming to assess its success rate and whether age can predict the result. Data on the study animals and success of the pairings were extracted from laboratory back-records: a total of 28 pairings was obtained. In addition, behavioural data were collected on six of the 28 pairs. Almost 80% of pairs were compatible beyond one week, and most of the fights occurred well within the first week after pair formation. Pairs in which one of the females was sexually immature (ie < 15 months) were significantly more compatible than pairs in which both females were post-pubertal. First encounters were characterised by sniffing of the unfamiliar monkey. Aggressive behaviours occurred frequently following pair formation but they were unidirectional, and in only two pairs was veterinary treatment required. This study shows that pairing of unfamiliar common marmoset females is a safe practice if one monkey is sexually immature, a result that supports observations of both group and pair formation in other primate species. However, given the potentially detrimental effects of removing young females from their natal groups, we argue that it is preferable to remove two sisters from their natal group when female pairs are required. However, when a single sexually mature female requires a pair mate so as to avoid single-housing and no mature sibling is available, an older, but still sexually immature, unfamiliar female that has had a normal development within the family should be considered as a pair mate.

In an effort to enhance welfare, behavioural management continually refines methods of non-human primate (NHP) care. Chimpanzees (Pan troglodytes) are one of the most cognitively complex captive NHPs and they have been observed to self-medicate in the wild. The population of captive chimpanzees in the US is aged (due to a breeding moratorium instituted in 1998) and will progressively require more medical care as they get older. To functionally simulate natural self-medication behaviour, provide chimpanzees with the opportunity to voluntarily participate in their own healthcare, and open new avenues of communication between caregivers and chimpanzees, we used a medication choice paradigm that allowed chimpanzees to choose their daily arthritis medication. We provided four arthritic, mobility-impaired chimpanzees with meloxicam or ibuprofen in blue or green Gatorade® to establish associations between the coloured drinks and the effects of the medications. We subsequently gave each chimpanzee a choice between the two medications. Behaviour was recorded using 15-min focal animal observations. Mobility was assessed using interactive mobility tests and a caregiver-rating system. One chimpanzee showed a medication preference (ibuprofen over meloxicam). The chimpanzees exhibited no significant behavioural or mobility differences over time, suggesting that ibuprofen and meloxicam may not differ significantly in their ability to alleviate arthritic symptoms. Whether or not the chimpanzees show a medication preference, the opportunity to make meaningful choices and the functional simulation of a complex behaviour, self-medication, is present when using this medication choice technique. Furthermore, the paradigm itself could have potential applications for additional medication options and treatment regimens.

Social role has been defined as a pattern of behaviour characteristic of a class of individuals within a group. The concept was developed by primatologists both to describe individual variation in behaviour in social groups and to be used in addition to hierarchy as a model for primate social organization. Cattle have been shown to express considerable individual variation in behaviour. Furthermore, cattle and primates show some similarities with respect to their social behaviour. This may indicate that the concept of social roles might be useful to those studying cattle behaviour. After a brief literature review it is concluded that the concept may indeed be applicable to cattle. The possible welfare implications of this are first, that it would offer a new approach for the study of individual differences in behaviour - important to the understanding of how animals cope with their environment in captivity. Second, it could help the understanding of social behaviour in domestic species. It is suggested that an interchange of ideas between primatologists and applied ethologists is needed.

The objective of this project was to collect scientific data to assist in the development of guidelines for the humane relocation of threatened and endangered arboreal non-human primate species. A troop of 31 Lowland Sykes monkeys (Cercopithecus mitis albotorquatus) was habituated to fruit bait for capture in a village and relocation to a previously selected suitable site in a protected forest reserve approximately 30 km away. Sixty-five percent (n = 20) of the animals were captured and relocated. This subgroup comprised one adult male, eight adult females, two subadult females, three juvenile males, four juvenile females and two infant males. Although the relocated group originated from one single group, post-translocation telemetry signals demonstrated that it split into two groups, which established themselves approximately 2–4 km apart in their new territory; the adult male eventually became solitary. The factors of importance for the successful capture and relocation of forest primates were found to include: proper understanding of troop home-range utilisation and of social bond organisation within the troop, method and period of habituation, method of release, suitability of the new habitat with respect to the ecological niche requirements of the species in question, and the period of post-relocation monitoring.

The presence of human visitors has been shown to affect the behaviour of several different mammalian species in a number of different zoos, but the behavioural changes observed are not always consistent with a simple ‘stressful influence’ explanation. Data for non-primate species are too sparse to draw meaningful conclusions; but for primates, the evidence reviewed in this paper allows several hypotheses to be tested. Neither a social facilitation nor an audience attraction hypothesis can be generally supported by the available studies. However, these studies are consistent with a general stressful influence hypothesis, although the extent of this influence is itself affected by other variables, notably species and housing differences. There is some evidence that chronic exposure to human audiences may lessen this stressful influence in some species; and in certain circumstances (notably where some members of the public throw food) the effect of the audience is almost an enriching one.