Sex differences in the acquisition of communicative competence by pigtail macaques (Macaca nemestrina)

Previous study of captive pigtail monkeys (Macaca nemestrina) revealed that victims of an attack by a group member employed one of four acoustically different recruitment calls (Gouzoules&Gouzoules: Animal Behaviour 37:383–401, 1989). The calls appear to provide allies with information pertinent to decisions about fight intervention. Each call was associated with an agonistic context distinguished by the relative rank of the opponent and the severity of the attack. Monkeys younger than 3 years of age were significantly less likely to use a contextually appropriate call than were older animals and their calls tended to be acoustically less like the prototype for a given context. Analyses reported on here revealed that, among juveniles, females were more proficient than males in both the proper contextual use and the production of these calls. These findings suggest parallels with human sex differences in the development of communicative competence. The evolutionary origins for these sex differences in macaque vocal development may be based in the different life history patterns males and females exhibit.     

Vocal discrimination of potential mates by female giant pandas (Ailuropoda melanoleuca)

In the current study, we used male giant panda (Ailuropoda melanoleuca) bleats in a habituation–discrimination paradigm to determine whether females discriminate between the vocalizations of different males. We found that females habituated to the bleats of a specific male showed a significant dishabituation when they were presented with bleats from a novel male. Further playbacks, in which we standardized the mean fundamental frequency (pitch) and amplitude modulation of male bleats, indicated that amplitude modulation is the key feature that females attend to when discriminating between male callers. Our results show that female giant pandas can discriminate between the vocalizations of potential mates and provide a platform for further studies investigating the functional role of caller identity in giant panda sexual communication.     

Selection for acoustic individuality within the vocal repertoire of wild chimpanzees

Individual primates typically produce acoustically distinct calls. To investigate the factors that facilitate the evolution of individual vocal signatures, we examined two components of the call repertoire of chimpanzees: the pant hoot and pant grunt. Pant hoots are long-distance signals whose recipients can be several hundred meters away, while pant grunts are short-range calls given to conspecifics within close visual range. Given their markedly different contexts of emission, we predicted that natural selection would favor the elaboration of individually distinctive acoustic features in pant hoots compared with pant grunts. Analyses of nine acoustic features revealed that pant hoots are more stereotyped within-individuals and variable between-individuals than pant grunts. These data are consistent with the hypothesis that selection may act to encode varying degrees of individuality in different components of the vocal repertoire of a single species.     

The evolution of nonhuman primate loud calls: Acoustic adaptation for long-distance transmission

Many nonhuman primates produce species-typical loud calls used to communicate between and within groups over long distances. Given their observed spacing functions, primate loud calls are likely to show acoustic adaptations to increase their propagation over distance. Here we evaluate the hypothesis that primates emit loud calls at relatively low sound frequencies to minimize their attenuation. We tested this hypothesis within and between species. First, we compared the frequencies of loud calls produced by each species with those of other calls from their vocal repertoires. Second, we investigated the relationship between loud call frequency and home range size across a sample of primate species. Comparisons indicated that primates produce loud calls at lower frequencies than other calls within their vocal repertoires. In addition, a significant negative relationship exists between loud call frequency and home range size among species. The relationship between call frequency and range size holds after controlling for the potentially confounding effects of body size and phylogeny. These results are consistent with the hypothesis that nonhuman primates produce loud calls at relatively low frequencies to facilitate their transmission over long distances.     

You talkin’ to me? Interactive playback is a powerful yet underused tool in animal communication research

Over the years, playback experiments have helped further our understanding of the wonderful world of animal communication. They have provided fundamental insights into animal behaviour and the function of communicative signals in numerous taxa. As important as these experiments are, however, there is strong evidence to suggest that the information conveyed in a signal may only have value when presented interactively. By their very nature, signalling exchanges are interactive and therefore, an interactive playback design is a powerful tool for examining the function of such exchanges. While researchers working on frog and songbird vocal interactions have long championed interactive playback, it remains surprisingly underused across other taxa. The interactive playback approach is not limited to studies of acoustic signalling, but can be applied to other sensory modalities, including visual, chemical and electrical communication. Here, I discuss interactive playback as a potent yet underused technique in the field of animal behaviour. I present a concise review of studies that have used interactive playback thus far, describe how it can be applied, and discuss its limitations and challenges. My hope is that this review will result in more scientists applying this innovative technique to their own study subjects, as a means of furthering our understanding of the function of signalling interactions in animal communication systems.     

Development in the Usage and Comprehension of Greeting Calls in a Free‐Ranging Group of Japanese Macaques (Macaca fuscata)

The main objective of this study is to clarify the developmental process involved in both the usage of greeting calls and the response to greeting calls by Japanese macaques. These greeting calls facilitate affiliative interactions by communicating benign intent. Specifically, individuals frequently emit greeting calls when interacting with less‐predictable individuals. Here, we examined whether the targets at which greeting calls are directed, along with associated behavioral responses, differed among the age classes, by conducting a cross‐sectional observation of females aged 0–5 yr and their mothers. We found that infant females showed a weak tendency to emit greeting calls at no specific receivers, unlike that by older females. Adult females emitted greeting calls more frequently when approaching unrelated females than related females. In contrast, young adult or juvenile females exhibited no significant difference in the proportion of the calls with related and unrelated conspecifics. Adult and young adult females were more likely to respond affiliatively to other individuals that approached using greeting calls compared with silent approaches, whereas juveniles did not exhibit different responses to the two types of approaches. This study showed that the target‐specific usage and affiliative response to greeting calls emerge with changes in the developmental stage. Furthermore, the fact that even young adults did not use greeting calls as adults indicates that the usage of greeting calls is modified in conjunction with the expansion of social relationships.     

Retraction of the mobile descended larynx during groaning enables fallow bucks (Dama dama) to lower their formant frequencies

A permanently descended larynx is found in humans and several other species of mammals. In addition to this, the larynx of species such as fallow deer is mobile and in males it can be retracted during vocalization. The most likely explanation for the lowered retractable larynx in mammals is that it serves to exaggerate perceived body size (size exaggeration hypothesis) by decreasing the formant frequencies of calls. In this study, we quantified for the first time the elongation of the vocal tract in fallow bucks during vocalization. We also measured the effect of this vocal tract length (VTL) increase on formant frequencies (vocal tract resonances) and formant dispersion (spacing of formants). Our results show that fallow bucks increase their VTL on average by 52% during vocalization. This elongation resulted in strongly lowered formant frequencies and decreased formant dispersion. There were minimal changes to formants 1 and 2 (−0.91 and +1.9%, respectively) during vocal tract elongation, whereas formants 3, 4 and 5 decreased substantially: 18.9, 10.3 and 13.6%, respectively. Formant dispersion decreased by 12.4%. Formants are prominent in deer vocalizations and are used by males to gain information on the competitive abilities of signallers. It remains to be seen whether females also use the information that formants contain for assessing male quality before mating.     

The anatomy of vocal divergence in North American Elk and European red deer

Loud and frequent vocalizations play an important role in courtship behavior in Cervus species. European red deer (Cervus elaphus) produce low‐pitched calls, whereas North American elk (Cervus canadensis) produce high‐pitched calls, which is remarkable for one of the biggest land mammals. Both species engage their vocal organs in elaborate maneuvers but the precise mechanism is unknown. Vocal organs were compared by macroscopic and microscopic dissection. The larynx is sexually dimorphic in red deer but not in elk. The laryngeal lumen is more constricted in elk, and narrows further during ontogeny. Several elements of the hyoid skeleton and two of four vocal tract segments are longer in red deer than in elk allowing greater vocal tract expansion and elongation. We conclude that elk submit the larynx and vocal tract to much higher tension than red deer, whereby, enormously stressed vocal folds of reduced effective length create a high resistance glottal source. The narrow, high impedance laryngeal vestibulum matches glottal and vocal tract impedance allowing maximum power transfer. In red deer longer and relaxed vocal folds create a less resistant glottal source and a wider vestibulum matches the low glottal impedance to the vocal tract, thereby also ensuring maximum power transfer. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.     

Geographic variation in the calls of wild chimpanzees: A reassessment

Male chimpanzees produce a species‐typical call, the pant hoot, to communicate to conspecifics over long‐distances. Calls given by males from the well‐known Gombe and Mahale populations typically consist of four different phases: an introduction, build‐up, climax, and let‐down. Recent observations suggest that chimpanzees living in the Kibale National Park, Uganda, consistently give calls that lack a build‐up and are thus qualitatively distinguishable acoustically from those made by other East African conspecifics. We analyzed additional recordings from Mahale and Kibale to re‐examine geographic variation in chimpanzee calls. Results indicate that males from both sites produce pant hoots containing all four parts of the call. Calls made by chimpanzees from the two populations, however, differ in quantitative acoustic measures. Specifically, males at Kibale initiate their calls with significantly longer elements and build‐up over briefer periods at slower rates than individuals from Mahale. Kibale males also deliver acoustically less variable calls than chimpanzees at Mahale. Although climax elements do not differ between populations in any single acoustic feature, discriminant function analysis reveals that acoustic variables can be used in combination to assign calls to the correct population at rates higher than that expected by chance. Ecological factors related to differences in habitat acoustics, the sound environment of the local biota, and body size are likely to account for these observed macrogeographic variations in chimpanzee calls. Am. J. Primatol. 47:133–151, 1999. © 1999 Wiley‐Liss, Inc.     

Preliminary observations on squirrel monkey (Saimiri oerstedi) vocalizations in Costa Rica

This study was an initial attempt to analyze quantitatively vocalizations from the Central American squirrel monkey, Saimiri oerstedi. Vocalizations were recorded in the wild at P. N. Corcovado (S. o. oerstedi). and at P. N. Manuel Antonio (S. o. citrinellus). Additional recordings were made from captive individuals of both subspecies. The acoustic structure of analyzed vocalizations resembled most closely the vocal repertoire of South American Saimiri with the “gothic arch” phenotype, in agreement with the prominent gothic arch facial pattern of S. oerstedi. New structural subtypes of the twitter (“dog-tooth twitter”) and the chuck (“bent-mast chuck”) not previously found in an extensive library of South American Saimiri sound spectrograms were documented. Calls used by older infants when socially separated and when approaching an adult male were essentially identical (sharing typical “isolation peep” structural features) but had significantly different duration and peak frequency. Analysis of recordings from an escaped captive female calling outside her compound over a 3-day period indicated the presence of numerous structural intermediates between typical chuck, twitter, and peep calls.     

Individuality in a contact call of the ringtailed lemur (Lemur catta)

A vocalization of the ringtailed lemur (Lemur catta) was examined for individual differences according to several temporal- and frequency-dependent variables. Vocalizations were tape recorded at the Duke University Primate Center (Durham, NC) and spectrographically analyzed. Significant differences were found in pair-wise comparisons of call structure among the study subjects, thus providing the physical basis for individual discrimination. A separate analysis comparing degree of kinship and vocal similarity revealed a positive but nonsignificant correlation between these two variables. This study represents an initial examination of vocal individuality in prosimian primates.     

Vocal communication as a function of differential rearing experiences inPan paniscus: A preliminary report

There is little evidence of vocal learning in nonhuman primates despite the well-documented abilities found in avian species. We describe the vocal repertoire of five bonobos (Pan paniscus), four of which live in a seminatural environment. The fifth subject, Kanzi, has been reared with humans during the course of language training. The data indicated that the four bonobos living in a seminatural environment exhibit a variety of species-typical vocalizations. In addition to producing all the species-typical vocalization, Kanzi produced four structurally unique vocalizations that were not heard among the other subjects. These data suggest that Kanzi has learned vocalizations that are novel due to his unique rearing experience. Discussion is focused on the flexibility of vocal communication and vocal comprehension inPan paniscus.     

Vocal communication of simulated pain

While evidence suggests that pain cries produced by human babies and other mammal infants communicate pain intensity, whether the pain vocalisations of human adults also encode pain intensity, and which acoustic characteristics influence listeners’ perceptions, remains unexplored. Here, we investigated how trained actors communicated pain by comparing the acoustic characteristics of nonverbal vocalisations expressing different levels of pain intensity (mild, moderate and severe). We then performed playback experiments to examine whether vocalisers successfully communicated pain intensity to listeners, and which acoustic characteristics were responsible for variation in pain ratings. We found that the mean and range of voice fundamental frequency (F0, perceived as pitch), the amplitude of the vocalisation, the degree of periodicity of the vocalisation and the proportion of the signal displaying non-linear phenomena all increased with the level of simulated pain intensity. In turn, these parameters predicted increases in listeners’ ratings of pain intensity. We also found that while different voice features contributed to increases in pain ratings within each level of expressed pain, a combination of these features explained an impressive amount of the variance in listeners’ pain ratings, both across (76%) and within (31–54%) pain levels. Our results show that adult vocalisers can volitionally simulate and modulate pain vocalisations to influence listeners’ perceptions of pain in a manner consistent with authentic human infant and nonhuman mammal pain vocalisations, and highlight potential for the development of a practical quantitative tool to improve pain assessment in populations unable to self-report their subjective pain experience.     

Vocal cooperation between the sexes in Little Spotted Kiwi Apteryx owenii

Sexual call dimorphism in birds is usually associated with sexual size dimorphism. Departures from this relationship can be used to infer call function, but research into inter‐sexual call differences, as with song function in general, has been restricted by a bias towards male passerines. The nocturnal and flightless New Zealand kiwi (Apterygidae) are acoustically similar but taxonomically and ecologically very different from other birds, so provide a contrast in exploring avian call function and evolution. However, kiwi acoustic ecology is poorly understood, with the calls of only one of the five kiwi species spectrally described, and acoustic differences between the sexes virtually unknown. We conducted the first bioacoustic study of Little Spotted Kiwi Apteryx owenii, and assessed sexual call dimorphism in this species. There were significant inter‐sexual differences in call temporal and frequency characteristics that were not related to size dimorphism. Contribution to duets and variation in temporal structure with call context also differed between the sexes. We suggest that these differences indicate divergent call function, with male calls more suited for territory defence, and female calls for pair contact. There was a striking lack of overlap in the frequency spectrum distributions of male and female calls, which was also unrelated to size and was further emphasized by the presence of formants in female calls. We propose that this provides evidence for inter‐sexual acoustic cooperation in call frequency, of a type which to our knowledge has not previously been described in birds. This may result from selection for enhanced joint resource defence in kiwi.     

Are men better than women at acoustic size judgements?

Formants are important phonetic elements of human speech that are also used by humans and non-human mammals to assess the body size of potential mates and rivals. As a consequence, it has been suggested that formant perception, which is crucial for speech perception, may have evolved through sexual selection. Somewhat surprisingly, though, no previous studies have examined whether sexes differ in their ability to use formants for size evaluation. Here, we investigated whether men and women differ in their ability to use the formant frequency spacing of synthetic vocal stimuli to make auditory size judgements over a wide range of fundamental frequencies (the main determinant of vocal pitch). Our results reveal that men are significantly better than women at comparing the apparent size of stimuli, and that lower pitch improves the ability of both men and women to perform these acoustic size judgements. These findings constitute the first demonstration of a sex difference in formant perception, and lend support to the idea that acoustic size normalization, a crucial prerequisite for speech perception, may have been sexually selected through male competition. We also provide the first evidence that vocalizations with relatively low pitch improve the perception of size-related formant information.