Hand preference in wild crab-eating capuchin monkeys (Sapajus libidinosus) in the coastal area of Northest Brazil.

Handedness is a fundamental human trait, although recent research, especially on nonhuman primates, has shown that it is displayed by other animals as well (e.g., chimpanzees, gorillas). In this study, we explore hand preference in wild crab-eating tufted capuchin monkeys (Sapajus libidinosus) inhabiting a mangrove forest located on the coastal area of Northeast Brazil (Maranhão State). Tufted capuchin monkeys at our site use facultatively wooden tools to crack open crabs. We observed hand preference in 12 subjects who spontaneously participated in experiment sessions, in which we provided crabs and tools on wooden platforms. We recorded (using events and bouts) two unimanual tasks, (tool or crab) grabbing and (tool or crab) pounding, and one bimanual task, crab pulling, where one hand kept the crab in place while the other pulled off parts of the crab. Hand preference increased with greater strength needed to perform the task and its complexity. While only 17%-25% of capuchins showed hand preference during grabbing, 44%-64% showed hand preference during pounding, and most subjects 64%-80% displayed a right-hand preference when performing the bimanual task, for which all lateralized individuals were right-handed. Hand preference did not vary between adults and juvenile individuals and was not consistent across tasks. Group-level hand preference was found only for the bimanual task, for which all lateralized individuals were right-handed. Our findings are in concordance with those of other primate studies showing the emergence of hemispheric specialization for bimanual actions, highlight the importance of conducting such studies on diverse type of tasks, and show the feasibility to conduct experimental manipulation under natural conditions.

Long-term home range stability provides foraging benefits in western gorillas.

OBJECTIVES: Long-term home range stability presumably emerges because familiarity with an area improves fitness through increased foraging efficiency, reduced predation risk, or reduced costs of intergroup aggression. While the use of spatial memory by primates has been widely demonstrated, few studies have examined whether long-term space use creates opportunities for interannual reuse of spatial knowledge. Here we examine the ranging behavior of western gorillas (Gorilla gorilla) to assess the degree of long-term site fidelity and the foraging consequences of reuse of space. METHODS: We measured interannual home range overlap over a 10-year period for a single group of gorillas at the Mondika Research Center, using both grid-based and kernel density estimation. By plotting the total area used over time, we identified periods of home-range stability and expansion. We compared foraging and ranging behavior in familiar versus unfamiliar areas, considering fruit trees visited, dietary diversity, and daily path length, to determine whether the lack of spatial knowledge in unfamiliar areas was associated with foraging costs. RESULTS: Average interannual home range overlap by the group remained high throughout the study. During periods of home range expansion, daily path lengths increased but not the number of fruit trees visited, suggesting that reduced familiarity with the area led to decreased foraging efficiency because individuals lacked prior knowledge of where to find resources. DISCUSSION: Western gorillas at Mondika exhibit long-term home range stability, presumably reflecting a strategy that relies on the use of spatial memory to increase foraging efficiency that is favored by their reliance on ephemeral fruit resources.

A novel attention-getting vocalization in zoo-housed western gorillas.

As a critical aspect of language, vocal learning is extremely rare in animals, having only been described in a few distantly related species. New evidence, however, extends vocal learning/innovation to the primate order, with zoo-housed chimpanzees and orangutans producing novel vocal signals to attract the attention of familiar human caregivers. If the ability to produce novel vocalizations as a means of navigating evolutionarily novel circumstances spans the Hominidae family, then we can expect to find evidence for it in the family's third genus, Gorilla. To explore this possibility, we conduct an experiment with eight gorillas from Zoo Atlanta to examine whether they use species-atypical vocalizations to get the attention of humans across three different conditions: just a human, just food, or a human holding food. Additionally, we survey gorilla keepers from other AZA-member zoos to compile a list of common attention-getting signals used by the gorillas in their care. Our experiment results indicated that Zoo Atlanta gorillas vocalized most often during the human-food condition, with the most frequently used vocal signal being a species-atypical sound somewhere between a sneeze and a cough (n = 28). This previously undescribed sound is acoustically different from other calls commonly produced during feeding (i.e., single grunts and food-associated calls). Our survey and analyses of recordings from other zoos confirmed that this novel attention-getting sound is not unique to Zoo Atlanta, although further work should be done to better determine the extent and patterns of transmission and/or potential independent innovation of this sound across captive gorilla populations. These findings represent one of the few pieces of evidence of spontaneous novel vocal production in non-enculturated individuals of this species, supporting the inclusion of great apes as moderate vocal learners and perhaps demonstrating an evolutionary function to a flexible vocal repertoire.

Who is there? Captive western gorillas distinguish human voices based on familiarity and nature of previous interactions.

The ability to recognize conspecifics by their acoustic signals is of crucial importance to social animals, especially where visibility is limited, because it allows for discrimination between familiar and unfamiliar individuals and facilitates associations with and the avoidance of particular conspecifics. Animals may also benefit from an ability to recognize and use the information coded into the auditory signals of other species. Companion species such as dogs, cats, and horses are able to discriminate between familiar and unfamiliar human voices; however, whether this ability is widespread across vertebrates is still unknown. Using playback experiments, we tested whether western gorillas living at Zoo Atlanta were able to discriminate between the voices of subgroups of people: i.e., unfamiliar individuals, familiar individuals with whom the gorillas had positive interactions, and familiar individuals with whom they had negative interactions. Gorillas responded significantly more often (longer gazing duration, higher gazing frequency, shorter latency, and larger number of distress behaviors) to the voices of unfamiliar and familiar-negative individuals than to those of familiar-positive individuals, indicating that they recognized the voices of subgroup of people based on familiarity and possibly the nature of the relationship with them. Future studies should determine whether this is also the case in the wild, where interspecific associations with humans are less intense than they are in captive settings.

Dominance style is a key predictor of vocal use and evolution across nonhuman primates.

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships.

Mixed-species associations and attempted mating suggest hybridization between purple-faced and tufted gray langurs of Sri Lanka.

Hybridization is increasingly recognized as an important mechanism of evolutionary change in the order Primates. Here, we present the first observational data supporting natural hybridization between the critically endangered purple-faced langur (Semnopithecus vetulus philbricki) and the threatened tufted gray langur (Semnopithecus priam thersites) in Kaludiyapokuna Forest Reserve in Sri Lanka. In one case study, we observed a long-term (> 1 year) mixed-species group consisting of one adult tufted gray langur male coexisting with seven adult purple-faced females. Although copulations were not observed, two infants were conceived during the male's tenure, and the coat color of one of these infants transitioned into that intermediate between those of the two langur species. The tufted gray langur male was also aggressive toward extra-group males of both species, as well as towards purple-faced juveniles within his group. However, we never witnessed the male exhibiting aggression towards the infants conceived during his tenure. In a second case study, a female purple-faced langur visited and sexually solicited a tufted gray langur male in a known study group of this species over the course of 2 days, in what resembled a sexual consortship. Taken together, the observed mixed-species association and attempted interspecific mating suggest that hybridization is very likely in these sympatric species. Genetic data are needed to confirm and determine the extent of hybridization in the dry zone of Sri Lanka where purple-faced langurs live in sympatry with tufted gray langurs.

Spatial cognition in western gorillas (Gorilla gorilla): an analysis of distance, linearity, and speed of travel routes.

Spatial memory allows animals to retain information regarding the location, distribution, and quality of feeding sites to optimize foraging decisions. Western gorillas inhabit a complex environment with spatiotemporal fluctuations of resource availability, prefer fruits when available, and travel long distances to reach them. Here, we examined movement patterns-such as linearity, distance, and speed of traveling-to assess whether gorillas optimize travel when reaching out-of-sight valued resources. Our results show that gorillas travel patterns are affected by the activity they perform next, the type of food they feed on, and their preference level to specific fruits, suggesting they are able to optimize foraging based on spatial knowledge of their resources. Additionally, gorillas left in the direction of the next resource as soon as they started traveling and decelerated before approaching food resources, as evidence that they have a representation of their exact locations. Moreover, home range familiarity did not influence gorillas' movement patterns, as travel linearity in the core and periphery did not differ, suggesting that they may not depend wholly on a network of paths to navigate their habitat. These results show some overlap with chimpanzees' spatial abilities. Differences between the two ape species exist, however, potentially reflecting more their differences in diet (degree of frugivory) rather than their cognitive abilities. Further studies should focus on determining whether gorillas are able to use shortcuts and/or approach the same goal from multiple directions to better identify the spatial abilities used by this species.

The context of chest beating and hand clapping in wild western gorillas (Gorilla gorilla gorilla).

Loud auditory gestures that are produced by repetitively percussing body parts are rare in primate repertoires and have been mostly observed in captive settings. Gorillas produce two of the most conspicuous long-range signals of this type: chest beating and hand clapping. Here we present the first systematic analysis of chest beating (n = 63) and hand clapping (n = 88) in wild western gorillas to assess the behavioral contexts in which they emerged, the flexibility of their use, and the age-sex classes that produced them. Data were collected at the Mondika Research Center, Republic of Congo, from a habituated gorilla group during two separate collection periods (June-August 2007; May 2009-June 2010). Our results show that both signals are highly context specific, with chest beating used only during display and/or play and hand clapping used only during vigilance and/or play. Age-sex classes differed in their use and production of these signals in that immature individuals used both signals only when playing, the male only used chest beating when displaying and never hand clapped, and adult females used both signals flexibly in two contexts instead of one. This study confirms previous anecdotal accounts of loud auditory gestures in western gorillas and adds crucial information on their flexibility across age categories. While chest beating has been described in both gorilla species, hand clapping as a way to communicate potential danger is unique to western gorillas. Further studies should focus on determining the variations in frequency and use across geographically distant populations.

Nutritional composition of the diet of the western gorilla (Gorilla gorilla): Interspecific variation in diet quality.

To meet nutritional needs, primates adjust their diets in response to local habitat differences, though whether these dietary modifications translate to changes in dietary nutrient intake is unknown. A previous study of two populations of the mountain gorilla (MG: Gorilla beringei) found no evidence for intraspecific variation in the nutrient composition of their diets, despite ecological and dietary differences between sites. One potential explanation is that nutritional variability in primate diets requires greater ecological divergence than what was captured between MG sites, underpinning environmental differences in the nutrient quality of plant foods. To test whether Gorilla exhibits interspecific variation in dietary composition and nutrient intake, we studied the composition and macronutrients of the western gorilla (WG: Gorilla gorilla) staple diets and compared them with published data from the two MG populations. We recorded feeding time and food intake of four adult female WGs from one habituated group over a period of 11 months (December 2004-October 2005) at the Mondika Research Center, Republic of Congo, allowing for assessment of seasonal patterns of nutrient intake. Staple diets of WGs and MGs diverged in their dietary and macronutrient composition. Compared to MGs, the staple diet of WGs (by intake) contained higher proportions of fruit (43%) and leaf (12%) and a lower proportion of herb (39%), resulting in a higher intake of total nonstructural carbohydrate and fiber and a lower intake of crude protein. Staple gorilla fruits and herbs differed in nutrient quality between sites. Gorillas exhibit nutritional flexibility that reflects ecological variation in the nutrient quality of plant foods. Since dietary quality typically affects rates of growth and reproduction in primates, our results suggest that interspecific differences in nutrient intake and food quality may shape differences in gorilla nutrient balancing and female life history strategies.

Behavioral Variation in Gorillas: Evidence of Potential Cultural Traits.

The question of whether any species except humans exhibits culture has generated much debate, partially due to the difficulty of providing conclusive evidence from observational studies in the wild. A starting point for demonstrating the existence of culture that has been used for many species including chimpanzees and orangutans is to show that there is geographic variation in the occurrence of particular behavioral traits inferred to be a result of social learning and not ecological or genetic influences. Gorillas live in a wide variety of habitats across Africa and they exhibit flexibility in diet, behavior, and social structure. Here we apply the 'method of exclusion' to look for the presence/absence of behaviors that could be considered potential cultural traits in well-habituated groups from five study sites of the two species of gorillas. Of the 41 behaviors considered, 23 met the criteria of potential cultural traits, of which one was foraging related, nine were environment related, seven involved social interactions, five were gestures, and one was communication related. There was a strong positive correlation between behavioral dissimilarity and geographic distance among gorilla study sites. Roughly half of all variation in potential cultural traits was intraspecific differences (i.e. variability among sites within a species) and the other 50% of potential cultural traits were differences between western and eastern gorillas. Further research is needed to investigate if the occurrence of these traits is influenced by social learning. These findings emphasize the importance of investigating cultural traits in African apes and other species to shed light on the origin of human culture.

Acoustic sequences in non-human animals: a tutorial review and prospectus.

Animal acoustic communication often takes the form of complex sequences, made up of multiple distinct acoustic units. Apart from the well-known example of birdsong, other animals such as insects, amphibians, and mammals (including bats, rodents, primates, and cetaceans) also generate complex acoustic sequences. Occasionally, such as with birdsong, the adaptive role of these sequences seems clear (e.g. mate attraction and territorial defence). More often however, researchers have only begun to characterise - let alone understand - the significance and meaning of acoustic sequences. Hypotheses abound, but there is little agreement as to how sequences should be defined and analysed. Our review aims to outline suitable methods for testing these hypotheses, and to describe the major limitations to our current and near-future knowledge on questions of acoustic sequences. This review and prospectus is the result of a collaborative effort between 43 scientists from the fields of animal behaviour, ecology and evolution, signal processing, machine learning, quantitative linguistics, and information theory, who gathered for a 2013 workshop entitled, 'Analysing vocal sequences in animals'. Our goal is to present not just a review of the state of the art, but to propose a methodological framework that summarises what we suggest are the best practices for research in this field, across taxa and across disciplines. We also provide a tutorial-style introduction to some of the most promising algorithmic approaches for analysing sequences. We divide our review into three sections: identifying the distinct units of an acoustic sequence, describing the different ways that information can be contained within a sequence, and analysing the structure of that sequence. Each of these sections is further subdivided to address the key questions and approaches in that area. We propose a uniform, systematic, and comprehensive approach to studying sequences, with the goal of clarifying research terms used in different fields, and facilitating collaboration and comparative studies. Allowing greater interdisciplinary collaboration will facilitate the investigation of many important questions in the evolution of communication and sociality.

The function of loud calls (Hoot Series) in wild western gorillas (Gorilla gorilla).

The use of loud vocal signals to reduce distance among separated social partners is well documented in many species; however, the underlying mechanisms by which the reduction of spacing occurs and how they differ across species remain unclear. Western gorillas (Gorilla gorilla) offer an opportunity to investigate these issues because their vocal repertoire includes a loud, long-distance call (i.e., hoot series) that is potentially used in within-group communication, whereas mountain gorillas use an identical call exclusively during intergroup encounters. First, we tested whether the hoot series functions as a contact/separation call. Second, we examined which individuals were more likely to reply and which party was more responsible for decreasing distance to identify the underlying mechanisms and cognitive implications of hoot series. We collected behavioral, spatial, and acoustic data on five adult gorillas over 15 months at the Mondika Research Center (Republic of Congo and CAR). Hoot series are individually distinct calls and given by both male and female gorillas when separated from each other. Following hooting, the distance between separated group members decreased significantly; thus we concluded that western gorillas use this call to reestablish group cohesion. The way in which proximity was achieved depended upon listeners replying or not to the caller. Replies may indicate a conflict between callers about intended travel direction, with vocal interchanges serving to negotiate a consensus. Although the acoustic features of vocal signals are highly constrained in closely related species, our results demonstrate that the function and usage of particular calls can be flexible.

Individual distinctiveness in call types of wild western female gorillas.

Individually distinct vocalizations play an important role in animal communication, allowing call recipients to respond differentially based on caller identity. However, which of the many calls in a species' repertoire should have more acoustic variability and be more recognizable is less apparent. One proposed hypothesis is that calls used over long distances should be more distinct because visual cues are not available to identify the caller. An alternative hypothesis proposes that close calls should be more recognizable because of their importance in social interactions. To examine which hypothesis garners more support, the acoustic variation and individual distinctiveness of eight call types of six wild western gorilla (Gorilla gorilla) females were investigated. Acoustic recordings of gorilla calls were collected at the Mondika Research Center (Republic of Congo). Acoustic variability was high in all gorilla calls. Similar high inter-individual variation and potential for identity coding (PIC) was found for all call types. Discriminant function analyses confirmed that all call types were individually distinct (although for call types with lowest sample size - hum, grumble and scream - this result cannot be generalized), suggesting that neither the distance at which communication occurs nor the call social function alone can explain the evolution of identity signaling in western gorilla communication.