A protocol for training group-housed rhesus macaques (Macaca mulatta) to cooperate with husbandry and research procedures using positive reinforcement.

There has been increased recognition of the 3Rs in laboratory animal management over the last decade, including improvements in animal handling and housing. For example, positive reinforcement is now more widely used to encourage primates to cooperate with husbandry procedures, and improved enclosure design allows housing in social groups with opportunity to escape and avoid other primates and humans. Both practices have become gold standards in captive primate care resulting in improved health and behavioural outcomes. However, training individuals and social housing may be perceived as incompatible, and so it is important to share protocols, their outcomes and suggestions for planning and improvements for future uptake. Here we present a protocol with link to video for training rhesus macaques (Macaca mulatta) housed in single-male - multi-female breeding groups to sit at individual stations in the social enclosure. Our aim was that the monkeys could take part in welfare-related cognitive assessments without the need for removal from the group or interference by group members. To do this we required most individuals in a group to sit by individual stations at the same time. Most of the training was conducted by a single trainer with occasional assistance from a second trainer depending on availability. We successfully trained 61/65 monkeys housed in groups of up to nine adults (plus infants and juveniles) to sit by their individual stationing tools for >30 s. Males successfully trained on average within 30 min (2 training sessions); females trained on average in 1 h 52 min ± 13min (7.44 sessions), with rank (high, mid, low) affecting the number of sessions required. On average, dominant females trained in 1 h 26 min ± 16 min (5.7 sessions), mid ranked females in 1 h 52 min ± 20min (7.45 sessions), and subordinate females took 2 h 44 min ± 36 min (10.9 sessions). Age, group size, reproductive status, temperament, and early maternal separation did not influence the number of sessions a monkey required to reach criterion. We hope this protocol will be useful for facilities worldwide looking to house their animals in naturalistic social groups without impacting on animal husbandry and management.

Evidence of a Vocalic Proto-System in the Baboon (Papio papio) Suggests Pre-Hominin Speech Precursors.

Language is a distinguishing characteristic of our species, and the course of its evolution is one of the hardest problems in science. It has long been generally considered that human speech requires a low larynx, and that the high larynx of nonhuman primates should preclude their producing the vowel systems universally found in human language. Examining the vocalizations through acoustic analyses, tongue anatomy, and modeling of acoustic potential, we found that baboons (Papio papio) produce sounds sharing the F1/F2 formant structure of the human [ɨ æ ɑ ɔ u] vowels, and that similarly with humans those vocalic qualities are organized as a system on two acoustic-anatomic axes. This confirms that hominoids can produce contrasting vowel qualities despite a high larynx. It suggests that spoken languages evolved from ancient articulatory skills already present in our last common ancestor with Cercopithecoidea, about 25 MYA.

Age effects on transfer index performance and executive control in baboons (Papio papio).

Reversal performance in the transfer index (TI) task is known to improve from prosimians to apes, suggesting that this task is a marker of cognitive evolution within the primate taxa (Rumbaugh, 1970). However, the cognitive processes recruited by this task remain unclear. In the present study, 19 socially-housed baboons (Papio papio) from 1.6 to 14.3 years of age were tested on a computerized version of the TI task, using an automated self-testing procedure. Age was a significant factor in the level of success, with the younger baboons outperforming the adults. The younger baboons learned the pre-reversal discrimination faster and improved their post-reversal performance more rapidly than adult baboons. As 17 of these baboons had already been tested in previous studies on inhibitory control and cognitive flexibility tasks, comparison across tasks provide indicators of the underlying cognitive processes. Age variations in performance were similar between the TI task and in an adaptation of the Wisconsin Card Sorting Task (WCST) measuring cognitive flexibility (Bonté et al., 2011). This contrasts previous results from a task requiring motor inhibitory control (Fagot et al., 2011). Therefore, these findings suggest that cognitive flexibility was a central component of the cognitive system that evolved within non-human primates. They also implicate a decline in executive control with age that begins during early adulthood in this baboon species.

Effects of freely accessible computerized test systems on the spontaneous behaviors and stress level of Guinea baboons (Papio papio).

Fagot and Paleressompoulle [Fagot and Paleressompoulle (2009) Behav Res Methods 41: 396-404] described a new automated learning device for monkeys (ALDM) to test the cognitive functions of nonhuman primates within their social groups. However, the impact of the ALDM procedure on animal well-being needs to be investigated. The present study assessed the consequences of ALDM testing on the behavioral repertoire of Guinea baboons (Papio papio) and their stress levels as inferred from measurements of saliva cortisol. Accessibility to ALDM test computers reduced the number of resting periods as well as the number of stereotypies. Lower cortisol levels were also found during ALDM testing. These findings and others demonstrate that ALDM testing has a positive impact on animal well-being and can be considered as a means for behavioral enrichment in captive primates.

Facial expressions in common marmosets (Callithrix jacchus) and their use by conspecifics.

Facial expressions have been studied mainly in chimpanzees and have been shown to be important social signals. In platyrrhine and strepsirrhine primates, it has been doubted that facial expressions are differentiated enough, or the species socially capable enough, for facial expressions to be part of their communication system. However, in a series of experiments presenting olfactory, auditory and visual stimuli, we found that common marmosets (Callithrix jacchus) displayed an unexpected variety of facial expressions. Especially, olfactory and auditory stimuli elicited obvious facial displays (such as disgust), some of which are reported here for the first time. We asked whether specific facial responses to food and predator-related stimuli might act as social signals to conspecifics. We recorded two contrasting facial expressions (fear and pleasure) as separate sets of video clips and then presented these to cage mates of those marmosets shown in the images, while tempting the subject with food. Results show that the expression of a fearful face on screen significantly reduced time spent near the food bowl compared to the duration when a face showing pleasure was screened. This responsiveness to a cage mate's facial expressions suggests that the evolution of facial signals may have occurred much earlier in primate evolution than had been thought.