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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.

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.

Animal traditions are increasingly threatened by human impact on natural habitats, posing a challenge to conservation policies. In northeastern Brazil, bearded capuchins (Sapajus libidinosus) inhabiting theCerrado-Caatingabiome of Fazenda Boa Vista use stone hammers and anvils to crack open palm nuts and other encased foods. The same species inhabiting the mangroves of Morro do Boi ambush crabs and process them using wooden hammers and anvils. These traditions are gradually acquired by young capuchins exposed to the tool using activity of skilled older group members. Changes in land cover have threatened the persistence of this species, where these rare tool-use traditions occur. To assess land cover changes over the past 30 years, we analyzed a time series of remotely sensed imagery and quantified trends in land cover and agriculture across both study sites. We also developed a predictive model to forecast future changes in land cover by 2034. Our results show that agriculture increased by more than 300% in both sites from 1987 to 2017. If current trends continue in Morro do Boi, only 42% of forest (0.15 km(2)) will remain, which is insufficient to support the resident population of capuchins. In Fazenda Boa Vista, most of the land suitable for agriculture has already been used for that purpose. If private conservation efforts at Fazenda Boa Vista are to be effective through 2034, agricultural use should not be expanded any further. Imminent erosion and loss of natural vegetation will exacerbate the current situation, even if agriculture is not expanded. Our study is an example of the need for conservation to take behavioral traditions into account, as they are not widespread across the species distribution.

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.

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.

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. Publisher PDF

Great apes and siamangs—but not humans—possess laryngeal air sacs, suggesting that they were lost over hominin evolution. The absence of air sacs in humans may hold clues to speech evolution, but little is known about their functions in extant apes. We investigated whether gorillas use their air sacs to produce the staccato ‘growling’ of the silverback chest beat display. This hypothesis was formulated after viewing a nature documentary showing a display by a silverback western gorilla (Kingo). As Kingo growls, the video shows distinctive vibrations in his chest and throat under which the air sacs extend. We also investigated whether other similarly staccato vocalizations—the whinny, sex whinny, and copulation grunt—might also involve the air sacs. To examine these hypotheses, we collected an opportunistic sample of video and audio evidence from research records and another documentary of Kingo’s group, and from videos of other gorillas found on YouTube. Analysis shows that the four vocalizations are each emitted in rapid pulses of a similar frequency (8–16 pulses per second), and limited visual evidence indicates that they may all occur with upper torso vibrations. Future research should determine how consistently the vibrations co-occur with the vocalizations, whether they are synchronized, and their precise location and timing. Our findings fit with the hypothesis that apes—especially, but not exclusively males—use their air sacs for vocalizations and displays related to size exaggeration for sex and territory. Thus changes in social structure, mating, and sexual dimorphism might have led to the obsolescence of the air sacs and their loss in hominin evolution.

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.

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.

This review was developed at an investigative workshop, “Analyzing Animal Vocal Communication Sequences” that took place on October 21–23 2013 in Knoxville, Tennessee, sponsored by the National Institute for Mathematical and Biological Synthesis (NIMBioS). NIMBioS is an Institute sponsored by the National Science Foundation, the U.S. Department of Homeland Security, and the U.S. Department of Agriculture through NSF Awards #EF-0832858 and #DBI-1300426, with additional support from The University of Tennessee, Knoxville. In addition to the authors, Vincent Janik participated in the workshop. D.T.B.’s research is currently supported by NSF DEB-1119660. M.A.B.’s research is currently supported by NSF IOS-0842759 and NIH R01DC009582. M.A.R.’s research is supported by ONR N0001411IP20086 and NOPP (ONR/BOEM) N00014-11-1-0697. S.L.DeR.’s research is supported by the U.S. Office of Naval Research. R.F.-i-C.’s research was supported by the grant BASMATI (TIN2011-27479-C04-03) from the Spanish Ministry of Science and Innovation. E.C.G.’s research is currently supported by a National Research Council postdoctoral fellowship. E.E.V.’s research is supported by CONACYT, Mexico, award number I010/214/2012.

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. Am J Phys Anthropol 155:379–391, 2014. © 2014 Wiley Periodicals, Inc.

Despite considerable interest in the vocal communication of non-human primates and its possible relevance to theories of language evolution, we know surprisingly little about how vocal communication varies between closely related species inhabiting differing environments. Here, we provide the first quantitative description of the vocal repertoire, calling rates, and call usage in wild western gorillas and compare it to the previous work on mountain gorilla vocal behavior. During 1572 h of focal follows (n = 533), we collected behavioral data on and recorded vocalizations (n = 2163) of eight individuals in one group at Mondika Research Center (Republic of Congo). We supplemented these data with opportunistic recordings of an additional adult male in a second group. We used discriminant function analysis to test how well calls can be categorized by their acoustic structure and used behavioral data to determine the typical usage of western gorilla call types. The vocal repertoire comprised of 17 call types. Twelve of 17 call types were given primarily in a single context. Our results were similar to previous studies of mountain gorillas in that grunts, and grumbles were used most frequently and the silverback male vocalized more frequently than other group members. However, compared to mountain gorillas, western gorillas used an additional call type (sex-whinny), used a second call type (hoot series) in a completely different context and by all age–sex classes, and used many more call types in a more context-specific fashion. Our study suggests that although vocal production is highly constrained by morphology and phylogeny, differing social and ecological conditions can yield differences in the use and function of calls, even between two closely related species such as western and mountain 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. peerReviewed

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.

In-vitro infection of normal human lymphocytes with HTLV-I (human T-cell lymphotropic retrovirus type I) has been carried out to study the target cell specificity and the kinetics of infection. Cord blood (CBL) and adult peripheral blood lymphocytes (PBL) have been co-cultivated with irradiated HTLV-I donor cells (MT2 and C91PL lines). Established (‘immortalized’) HTLV-I positive cell lines were obtained only from CBL: in comparison with PBL, a less mature phenotype of T-cell subsets and a lower interferon-γ production was evidenced in CBL. A progressive variation of differentiation antigen representation and of exogenous T-cell growth factor (TCGF, interleukin-2, IL-2) medium concentration was observed with increasing time from infection. The four established lines obtained showed a predominant T3+, T4+, T8−, Tac+ phenotype and a reduced TCGF requirement. Studies on kinetics of HTLV-I infection showed that p19 and p24 viral antigens became expressed after a lag phase of 5 weeks. DNA Southern blot analysis indicated that a shift from polyclonal to monoclonal pattern of proviral integration occurred with time of culture, both complete and defective copies being transmitted from donor to recipient cells.