Do zoo-housed primates retreat from crowds? A simple study of five primate species.

An animal's welfare state is directly influenced by the mental state, which is shaped by experiences within the environment throughout the animal's life. For zoo-housed animals, visitors to the zoo are a large part of that environment and a fluctuating influence within it. This study examines the impact of zoo visitors on the space use of five species of zoo-housed primates (Eastern black-and-white colobus monkeys, Colobus guereza, n = 5, Allen's swamp monkeys, Allenopithecus nigroviridis, n = 2, DeBrazza's monkeys, Cercopithecus neglectus, n = 3, Bolivian gray titi monkeys, Callicebus donacophilus, n = 3, and crowned lemurs, Eulemur coronatus, n = 3). Specifically, we considered whether primates' distance from visitor areas changed as crowd sizes increased. Data were collected using the ZooMonitor app. Observers recorded spatial coordinates for each animal over periods ranging from 12 to 32 months. Data were analyzed using two types of regression models (linear and logistic) to examine the influence of visitors on the location of the primates. Both analyses revealed a statistically significant but small decrease in primate distance from visitor viewing glass as the number of visitors increased. Behavioral indicators of welfare were also unaffected by the presence of visitors. These results suggest that, with additional validation, distance from visitors may be one promising, simple way to evaluate the influence of visitors on primate welfare.

The structure of species discrimination signals across a primate radiation.

Discriminating conspecifics from heterospecifics can help avoid costly interactions between closely related sympatric species. The guenons, a recent primate radiation, exhibit high degrees of sympatry and form multi-species groups. Guenons have species-specific colorful face patterns hypothesized to function in species discrimination. Here, we use a machine learning approach to identify face regions most essential for species classification across fifteen guenon species. We validate these computational results using experiments with live guenons, showing that facial traits critical for accurate classification influence selective attention toward con- and heterospecific faces. Our results suggest variability among guenon species in reliance on single-trait-based versus holistic facial characteristics for species discrimination, with behavioral responses and computational results indicating variation from single-trait to whole-face patterns. Our study supports a role for guenon face patterns in species discrimination, and shows how complex signals can be informative about differences between species across a speciose and highly sympatric radiation.

Death of the (traveling) salesman: primates do not show clear evidence of multi-step route planning.

Several comparative studies have linked larger brain size to a fruit-eating diet in primates and other animals. The general explanation for this correlation is that fruit is a complex resource base, consisting of many discrete patches of many species, each with distinct nutritional traits, the production of which changes predictably both within and between seasons. Using this information to devise optimal spatial foraging strategies is among the most difficult problems to solve in all of mathematics, a version of the famous Traveling Salesman Problem. Several authors have suggested that primates might use their large brains and complex cognition to plan foraging strategies that approximate optimal solutions to this problem. Three empirical studies have examined how captive primates move when confronted with the simplest version of the problem: a spatial array of equally valuable goals. These studies have all concluded that the subjects remember many food source locations and show very efficient travel paths; some authors also inferred that the subjects may plan their movements based on considering combinations of three or more future goals at a time. This analysis re-examines critically the claims of planned movement sequences from the evidence presented. The efficiency of observed travel paths is largely consistent with use of the simplest of foraging rules, such as visiting the nearest unused "known" resource. Detailed movement sequences by test subjects are most consistent with a rule that mentally sums spatial information from all unused resources in a given trial into a single "gravity" measure that guides movements to one destination at a time.

Female putty-nosed monkeys use experimentally altered contextual information to disambiguate the cause of male alarm calls.

Many animal vocal signals are given in a wide range of contexts which can sometimes have little in common. Yet, to respond adaptively, listeners must find ways to identify the cause of a signal, or at least rule out alternatives. Here, we investigate the nature of this process in putty-nosed monkeys, a forest primate. In this species, adult males have a very restricted repertoire of vocalizations which are given in response to a wide variety of events occurring under conditions of limited visibility. We carried out a series of field playback experiments on females (N = 6) in a habituated group in Gashaka Gumti National Park, Nigeria, in which male alarm/loud calls were presented either alone, or following acoustic information that simulated the occurrence of natural disturbances. We demonstrate that listeners appear to integrate contextual information in order to distinguish among possible causes of calls. We conclude that, in many cases, pragmatic aspects of communication play a crucial role in call interpretation and place a premium on listeners' abilities to integrate information from different sources.

Validation of an auditory sensory reinforcement paradigm: Campbell's monkeys (Cercopithecus campbelli) do not prefer consonant over dissonant sounds.

The central position and universality of music in human societies raises the question of its phylogenetic origin. One of the most important properties of music involves harmonic musical intervals, in response to which humans show a spontaneous preference for consonant over dissonant sounds starting from early human infancy. Comparative studies conducted with organisms at different levels of the primate lineage are needed to understand the evolutionary scenario under which this phenomenon emerged. Although previous research found no preference for consonance in a New World monkey species, the question remained opened for Old World monkeys. We used an experimental paradigm based on a sensory reinforcement procedure to test auditory preferences for consonant sounds in Campbell's monkeys (Cercopithecus campbelli campbelli), an Old World monkey species. Although a systematic preference for soft (70 dB) over loud (90 dB) control white noise was found, Campbell's monkeys showed no preference for either consonant or dissonant sounds. The preference for soft white noise validates our noninvasive experimental paradigm, which can be easily reused in any captive facility to test for auditory preferences. This would suggest that human preference for consonant sounds is not systematically shared with New and Old World monkeys. The sensitivity for harmonic musical intervals emerged probably very late in the primate lineage.

Hand preference and its flexibility according to the position of the object: a study in cercopithecines examining spontaneous behaviour and an experimental task (the Bishop QHP task).

The extant literature on manual laterality in non-human primates is inconclusive, plagued by inconsistent or contradictory findings and by disturbing methodological issues (e.g. uncontrolled influential factors, comparability issues). The present study examined hand preference and its flexibility in 15 red-capped mangabeys (C. t. torquatus) and 13 Campbell's monkeys (C. c. campbelli), two species that differ in their degree of arboreality. We investigated the influence of the spatial position of the object on hand preference for reaching. We considered spontaneous behaviour (reaching for food during daily feeding) and an experimental task: the QHP task. The QHP is a task that is used in humans. This is a simple reaching task that involves high spatial constraints on hand use. In our study, the subject had to reach for items that were placed on a semi-circle in front of it on five positions, including in the centre position, in the ipsilateral space and in the contralateral space. We assessed hand preference for reaching in front (baseline condition), and we examined how this preference changed when reaching in lateral positions. For reaching in front, about half of the subjects were lateralized and no group-level bias occurred, for both spontaneous and experimental conditions. When considering reaching in the lateral positions, we observed that the position of the object influenced hand use: individuals used the hand that was closest to the object. The results are discussed in relation to previous findings in humans and in non-human primates and regarding theories on handedness and flexibility of hand preference.

Call combinations in monkeys: compositional or idiomatic expressions?

Syntax is widely considered the feature that most decisively sets human language apart from other natural communication systems. Animal vocalisations are generally considered to be holistic with few examples of utterances meaning something other than the sum of their parts. Previously, we have shown that male putty-nosed monkeys produce call series consisting of two call types in response to different events. They can also be combined into short sequences that convey a different message from those conveyed by either call type alone. Here, we investigate whether 'pyow-hack' sequences are compositional in that the individual calls contribute to their overall meaning. However, the monkeys behaved as if they perceived the sequence as an idiomatic expression rather than decoding the sequence. Nonetheless, while this communication system lacks the generative power of syntax it enables callers to increase the number of messages that can be conveyed by a small and innate call repertoire.

Context-related call combinations in female Diana monkeys.

Non-human primates possess species-specific repertoires of acoustically distinct call types that can be found in adults in predictable ways. Evidence for vocal flexibility is generally rare and typically restricted to acoustic variants within the main call types or sequential production of multiple calls. So far, evidence for context-specific call sequences has been mainly in relation to external disturbances, particularly predation. In this study, we investigated extensively the vocal behaviour of free-ranging and individually identified Diana monkeys in non-predatory contexts. We found that adult females produced four vocal structures alone ('H', 'L', 'R' and 'A' calls, the latter consisting of two subtypes) or combined in non-random ways ('HA', 'LA' and 'RA' call combinations) in relation to ongoing behaviour or external events. Specifically, the concatenation of an introductory call with the most frequently emitted and contextually neutral 'A' call seems to function as a contextual refiner of this potential individual identifier. Our results demonstrate that some non-human primates are able to increase the effective size of their small vocal repertoire not only by varying the acoustic structure of basic call types but also by combining them into more complex structures. We have demonstrated this phenomenon for a category of vocalisations with a purely social function and discuss the implications of these findings for evolutionary theories of primate vocal communication.

Age- and sex-specific patterns of vocal behavior in De Brazza's monkeys (Cercopithecus neglectus).

Although vocal production is strongly genetically determined in nonhuman primates, vocal usage is more likely to be influenced by experience. Nonetheless, sex differences in both production and usage can be found in the vocal repertoire of adults, but little attention has been paid to their ontogeny. Here, we provide the first comprehensive analysis of the vocal repertoire of De Brazza's monkeys (Cercopithecus neglectus), with particular attention to age- and sex-specific patterns. This species has special interest because it is the only monogamous species of guenons, but it nevertheless shares the strong sexual morphological and behavioral dimorphism seen in other guenons. A structurally based classification of calls recorded in 23 captive individuals has been cross-validated by an analysis of the associated contexts of emission. We identified sound units that could be uttered alone or concatenated to form 10 call types, including only three types shared by all age-sex-classes. Both age- and sex-discrepancy in terms of phonation could be explained by maturational changes and morphological dimorphism. In general, call production and usage parallel those seen in other guenons, suggesting that phylogeny and sexual dimorphism play important roles in vocal communication in this species. However, the boundary between adult male and female vocal repertoires appeared to be less strict than previously reported, suggesting that both sexes have the capacity to produce calls of the other sex but that social roles may constrain this expression. Similarly, age-specific vocal patterns would reflect respective social roles, and experience to some extent. Finally, calling rates would reflect age-/sex-specific degree of involvement in intragroup social networks. These findings highlight the relative importance of phylogeny, morphology, and social system on the shaping of individual repertoires in nonhuman primates.

Acoustic variability and social significance of calls in female Campbell's monkeys (Cercopithecus campbelli campbelli).

Although the vocal repertoire of nonhuman primates is strongly constrained by genetic, a growing number of studies evidence socially determined flexibility. According to Snowdon et al. [Social Influences on Vocal Development (University Press, Cambridge, 1997), pp. 234-248], calls with a higher social function (affiliative or agonistic) would be expected to show more flexibility than lesser social calls. Owren and Rendall [Evol. Anthropol., 10, 58-71 (2001)] nuanced this by defending a structure-function relationship. Calls with particular acoustic properties, which directly influence the listener's affect, would be less individually distinctive than calls involved in an affective conditioning process. These hypotheses were tested in Campbell's monkeys using telemetric recordings. This is the first detailed description of female Campbell's monkeys' vocal repertoire emphasizing a possible relationship between social function and flexibility level. The vocal repertoire displayed an "arborescent" organization (call type, subtype, and variants). The highest number of subtypes and the greatest acoustic variability, within and among individuals, were found in calls associated with the highest affiliative social value. However, calls associated with agonism were the most stereotyped, whereas less social alarm calls were intermediate. This only partially validate the hypothesis of Snowdon et al. In accordance with Owren and Rendall's hypotheses, the level of individual distinctiveness was minimum for noisy pulsed calls and maximum for calls involved in affiliative interactions.

Status of diurnal primate populations at the former settlement of a displaced village in Cameroon.

To understand whether or not primate populations recover in areas of abandoned human settlements, data are required that allow for site-specific comparison over time. Here, we present baseline information on the presence/absence and relative abundance of primate species at the abandoned settlement of the Ekundukundu village, relocated out of the Korup National Park in 2000. Between July 2007 and March 2008, 62 km of transects was surveyed for sightings and calls of primates. All eight species of diurnal primates reported in the KNP were confirmed: Cercopithecus nictitans ludio, C. mona, C. erythrotis camerunensis, C. pogonias, Procolobus pennantii preussi, Cercocebus torquatus, Mandrillus leucophaeus leucophaeus, and Pan troglodytes vellerosus. At old Ekundukundu, C. nictitans accounted for 65% of all primate group sightings. Overall, sighting frequency of primates (0.55 groups/km) was not significantly different from other park sectors surveyed by a previous observer (J. Linder) in 2004-2005. The data reported here will be useful in the long-term monitoring of primate populations in regenerating forest habitats of earlier human settlements.

Attention to elders' voice in non-human primates.

The observed respect and attention to elders' speech in traditional cultures appears to have a 'universal' component which questions its possible biological bases. Animals present differential attention to the vocalizations of other individuals according to their characteristics but little is known about the potential propensity to pay more attention to vocalizations of elders. On the basis of several hundreds of vocal exchanges recorded, here we show that aged female Campbell's monkeys (Cercopithecus campbelli), despite being significantly less 'loquacious' than their younger adult counterparts, elicit many more responses when calling. These findings show that attention to elders' vocal production appears in non-human primates, leading to new lines of questioning on human culture and language evolution.

Examining deep litter as environmental enrichment for a family group of Wolf's guenons, Cercopithecus wolfi.

Manipulable substrates promote species-typical behavior and decrease abnormal behavior in a variety of primate species. However, the effects of providing litter to arboreal primates are not as well studied, and there is little information specifically concerning enrichment for guenons. To inform the captive management of an under-studied species, we evaluated deep litter substrate as environmental enrichment for a family group of Wolf's guenons, Cercopithecus wolfi. We expected it to promote species-typical behavior and to act as an intervention by reducing aggressive behaviors targeted toward a juvenile group member by his parents. We compared the guenons' behavior during baseline periods in which normal husbandry routines were followed to periods when the entire floor of their enclosure was covered with 30 cm of straw or wood wool. We then evaluated the group's preference between litters by comparing their relative use. The guenons spent more time feeding and were more active during both litter conditions, but relative to their respective baselines, they spent more time examining straw and less time examining wood wool. Straw, but not wood wool, promoted some affiliative behavior as well as greater tolerance of the juvenile's social proximity to others. However, the addition of deep litter did not ameliorate patterns of agonistic behavior among our subjects. Our results suggest that straw conferred greater behavioral benefits than wood wool as a deep litter substrate for this guenon group and may constitute a form of environmental enrichment for this species.

Sex and age differences in juvenile social priorities in female philopatric, nondespotic blue monkeys.

Juveniles should choose social partners on the basis of both current and future utility. Where one sex is philopatric, one expects members of that sex to develop greater and sex-typical social integration with group-mates over the juvenile period. Where a partner's position in a dominance hierarchy is not associated with services it can provide, one would not expect juveniles to choose partners based on rank, nor sex differences in rank-based preferences. We tested these ideas on 39 wild juvenile (3.2-7.4 years) blue monkeys (Cercopithecus mitis stuhlmanni), cercopithecines with strict female philopatry and muted hierarchies. We made focal animal observations over 6 months, and computed observed:expected amounts of proximity time, approaches and grooming given to various social partners. Overall, our results agree with the hypothesis that juvenile blue monkeys target social partners strategically. Spatial proximity, approaches and active grooming showed similar patterns regarding juvenile social preferences. Females were far more sociable than males, groomed more partners, reciprocated grooming more frequently, and preferred-while males avoided-infants as partners. Older juveniles (5-7 years) spent more time than younger juveniles (3-4 years) near others, and older females were especially attracted to infants. Close kin, especially mothers and less consistently adult sisters, were attractive to both male and female juveniles, regardless of age. Both sexes also preferred same-sex juveniles as social partners while avoiding opposite-sex peers. Juveniles of both sexes and ages generally neither preferred nor avoided nonmaternal adult females, but all juveniles avoided adult males. Partner's rank had no consistent effect on juveniles' preference, as expected for a species in which dominance plays a weak role. Juveniles' social preferences likely reflect both future and current benefits, including having tolerant adult kin to protect them against predators and conspecifics, same-sex play partners, and, for females, infants on which to practice mothering skills. Am. J. Primatol. 72:193-205, 2010. (c) 2009 Wiley-Liss, Inc.

Predation increases acoustic complexity in primate alarm calls.

According to most accounts, alarm calling in non-human primates is a biologically hardwired behaviour with signallers having little control over the acoustic structure of their calls. In this study, we compared the alarm calling behaviour of two adjacent populations of Diana monkeys at Taï forest (Ivory Coast) and Tiwai Island (Sierra Leone), which differ significantly in predation pressure. At Taï, monkeys regularly interact with two major predators, crowned eagles and leopards, while at Tiwai, monkeys are only hunted by crowned eagles. We monitored the alarm call responses of adult male Diana monkeys to acoustic predator models. We found no site-specific differences in the types of calls given to eagles, leopards and general disturbances, but there were consistent differences in how callers assembled calls into sequences. At Tiwai, males responded to leopards and general disturbances in the same way, while at Taï, males discriminated by giving call sequences that differed in the number of component calls. Responses to eagles were identical at both sites. We concluded that Diana monkeys are predisposed to use their repertoire in context-specific ways, but that ontogenetic experience determines how individual calls are assembled into meaningful sequences.

Cheek pouch use, predation risk, and feeding competition in blue monkeys (Cercopithecus mitis stuhlmanni).

The adaptive function of cheek pouches in the primate subfamily Cercopithecinae remains unresolved. By analyzing the circumstances of cheek pouch use, we tested two hypotheses for the evolution of cercopithecine cheek pouches proposed in earlier studies: (1) cheek pouches reduce vulnerability to predation, and (2) cheek pouches increase feeding efficiency by reducing competition. We studied two groups of wild blue monkeys (Cercopithecus mitis stuhlmanni) in the Kakamega Forest, Kenya, conducting focal observations of feeding individuals. Monkeys were less exposed while emptying their cheek pouches than filling them, supporting the predation-avoidance hypothesis. We investigated several measures of competitive threat, but only one supported the competition-reduction hypothesis: when the nearest neighbor's rank increased, subjects were more likely to increase than to decrease cheek pouch use. Overall, our findings supported the predation-avoidance hypothesis more strongly than the competition-reduction hypothesis. We suggest that variation in cheek pouch use may reflect differing behavioral strategies used by cercopithecines to mitigate competition and predation, as well as factors such as resource size and distribution, home range size, and travel patterns.

Male blue monkeys alarm call in response to danger experienced by others.

Male blue monkeys (Cercopithecus mitis stuhlmanni) of Budongo Forest, Uganda, produce two acoustically distinct alarm calls: hacks to crowned eagles (Stephanoaetus coronatus) and pyows to leopards (Panthera pardus) and a range of other disturbances. In playback experiments, males responded to leopard growls exclusively with a series of pyows and to eagle shrieks predominantly with hacks. Responses to playbacks of these alarm call series matched the responses to the corresponding predators, suggesting that the calls conveyed something about the nature of the threat. When responding to a series of hacks, indicating an eagle, males responded predominately with hacks, but produced significantly more calls if their group members were close to the playback stimulus than far away, regardless of their own position. When responding to a series of pyows, indicating a range of disturbances, males responded with pyows, but call rates were independent of the distance of other group members. The results suggest that males took into account the degree of danger experienced by other group members.

Female social relationships in a captive group of Campbell's monkeys (Cercopithecus campbelli campbelli).

A study group of Campbell's monkeys (Cercopithecus c. campbelli) provided data on affiliative and agonistic relationships between females. Over a period of two years (involving 111 hr), we conducted observations of a captive group which had a composition similar to wild groups. We were able to identify a monitor-adjust social system with frequent affiliative interactions, directed gazing and avoidances rather than aggressive acts. We described long-term differentiated affiliative bonds: adult females interacting more often with some group mates than others, especially if they were relatives. Interactions between matrilines concerned essentially play and young adult females. We found a significant linear hierarchy of dominance with rare reversals and a stable intermatriline dominance. In contrast to other single-male groups, our adult male was socially integrated into the group although this may have been because of the housing conditions. Comparisons with the social organization of other captive and wild guenon groups are discussed.