Pied tamarins change their vocal behavior in response to noise levels in the largest city in the Amazon.

Many animal species depend on sound to communicate with conspecifics. However, human-generated (anthropogenic) noise may mask acoustic signals and so disrupt behavior. Animals may use various strategies to circumvent this, including shifts in the timing of vocal activity and changes to the acoustic parameters of their calls. We tested whether pied tamarins (Saguinus bicolor) adjust their vocal behavior in response to city noise. We predicted that both the probability of occurrence and the number of long calls would increase in response to anthropogenic noise and that pied tamarins would temporally shift their vocal activity to avoid noisier periods. At a finer scale, we anticipated that the temporal parameters of tamarin calls (e.g., call duration and syllable repetition rate) would increase with noise amplitude. We collected information on the acoustic environment and the emission of long calls in nine wild pied tamarin groups in Manaus, Brazil. We found that the probability of long-call occurrence increased with higher levels of anthropogenic noise, though the number of long calls did not. The number of long calls was related to the time of day and the distance from home range borders-a proxy for the distance to neighboring groups. Neither long-call occurrence nor call rate was related to noise levels at different times of day. We found that pied tamarins decreased their syllable repetition rate in response to anthropogenic noise. Long calls are important for group cohesion and intergroup communication. Thus, it is possible that the tamarins emit one long call with lower syllable repetition, which might facilitate signal reception. The occurrence and quantity of pied tamarin' long calls, as well as their acoustic proprieties, seem to be governed by anthropogenic noise, time of the day, and social mechanisms such as proximity to neighboring groups.

Twin vocal folds as a novel evolutionary adaptation for vocal communications in lemurs.

Primates have varied vocal repertoires to communicate with conspecifics and sometimes other species. The larynx has a central role in vocal source generation, where a pair of vocal folds vibrates to modify the air flow. Here, we show that Madagascan lemurs have a unique additional pair of folds in the vestibular region, parallel to the vocal folds. The additional fold has a rigid body of a vocal muscle branch and it is covered by a stratified squamous epithelium, equal to those of the vocal fold. Such anatomical features support the hypothesis that it also vibrates in a manner like the vibrations that occur in the vocal folds. To examine the acoustic function of the two pairs of folds, we made a silicone compound model to demonstrate that they can simultaneously vibrate to lower the fundamental frequency and increase vocal efficiency. Similar acoustic effects are achieved using different features of the larynx for the other primates, e.g., by vibrating multiple sets of ventricular folds in several species and further by an evolutionary modification of enlarged larynx in howler monkeys. Our multidisciplinary approaches found that these functions were acquired through a unique evolutionary adaptation of the twin vocal folds in Madagascan lemurs.

Conceptualization, context, and comparison are key to understanding the evolution of fear.

The fearful ape hypothesis proposes that heightened fearfulness in humans is adaptive. However, despite its attractive anthropocentric narrative, the evidence presented for greater fearfulness in humans versus other apes is not sufficient to support this claim. Conceptualization, context, and comparison are strongly lacking in Grossmann's proposal, but are key to understanding variation in the fear response among individuals and species.

Evolutionary loss of complexity in human vocal anatomy as an adaptation for speech.

Human speech production obeys the same acoustic principles as vocal production in other animals but has distinctive features: A stable vocal source is filtered by rapidly changing formant frequencies. To understand speech evolution, we examined a wide range of primates, combining observations of phonation with mathematical modeling. We found that source stability relies upon simplifications in laryngeal anatomy, specifically the loss of air sacs and vocal membranes. We conclude that the evolutionary loss of vocal membranes allows human speech to mostly avoid the spontaneous nonlinear phenomena and acoustic chaos common in other primate vocalizations. This loss allows our larynx to produce stable, harmonic-rich phonation, ideally highlighting formant changes that convey most phonetic information. Paradoxically, the increased complexity of human spoken language thus followed simplification of our laryngeal anatomy.

From Soundwave to Soundscape: A Guide to Acoustic Research in Captive Animal Environments.

Sound is a complex feature of all environments, but captive animals' soundscapes (acoustic scenes) have been studied far less than those of wild animals. Furthermore, research across farms, laboratories, pet shelters, and zoos tends to focus on just one aspect of environmental sound measurement: its pressure level or intensity (in decibels). We review the state of the art of captive animal acoustic research and contrast this to the wild, highlighting new opportunities for the former to learn from the latter. We begin with a primer on sound, aimed at captive researchers and animal caregivers with an interest (rather than specific expertise) in acoustics. Then, we summarize animal acoustic research broadly split into measuring sound from animals, or their environment. We guide readers from soundwave to soundscape and through the burgeoning field of conservation technology, which offers new methods to capture multiple features of complex, gestalt soundscapes. Our review ends with suggestions for future research, and a practical guide to sound measurement in captive environments.

Progress without exclusion in the search for an evolutionary basis of music.

Mehr et al.'s hypothesis that the origins of music lie in credible signaling emerges here as a strong contender to explain early adaptive functions of music. Its integration with evolutionary biology and its specificity mark important contributions. However, much of the paper is dedicated to the exclusion of popular alternative hypotheses, which we argue is unjustified and premature.

Scent Marks Signal Species, Sex, and Reproductive Status in Tamarins (Saguinus spp., Neotropical Primates).

Olfactory communication is an important mediator of social interactions in mammals, thought to provide information about an individual's identity and current social, reproductive, and health status. In comparison with other taxa such as carnivores and rodents, few studies have examined primate olfactory communication. Tamarins (Callitrichidae) conspicuously deposit odorous secretions, produced by specialized scent glands, in their environment. In this study, we combined behavioral and chemical data on captive cotton-top tamarins, Saguinus oedipus, and bearded emperor tamarins, S. imperator subgrisescens, to examine the role of olfactory communication in the advertisement of species, sex, and reproductive status. We observed no difference in scent-marking behavior between species; however, females marked more frequently than males, and reproductive individuals more than non-reproductive ones. In addition, tamarins predominantly used their anogenital gland when scent-marking, followed by the suprapubic gland. We collected swabs of naturally deposited tamarin anogenital scent marks, and analyzed these samples using headspace gas chromatography-mass spectrometry. Despite a limited sample size, we established differences in tamarin anogenital mark chemical composition between species, sex and reproductive status, and identified 41 compounds. The compounds identified, many of which have been reported in previous work on mammalian semiochemistry, form targets for future bioassay studies to identify semiochemicals. Our non-invasive method for collecting deposited scent marks makes it a promising method for the study of olfactory communication in scent-marking animal species, applicable to field settings and for the study of elusive animals.

On the trail of primate scent signals: A field analysis of callitrichid scent-gland secretions by portable gas chromatography-mass spectrometry.

Chemosignals are mediators of social interactions in mammals, providing con- and hetero-specifics with information on fixed (e.g., species, sex, group, and individual identity) and variable (e.g., social, reproductive, and health status) features of the signaler. Yet, methodological difficulties of recording and quantifying odor signals, especially in field conditions, have hampered studies of natural systems. We present the first use of the Torion® portable gas chromatography-mass spectrometry (GC-MS) instrument for in situ chemical analysis of primate scents. We collected and analyzed swab samples from the scent glands and skin from 13 groups (57 individuals) of two sympatric species of wild emperor tamarins, Saguinus imperator, and Weddell's saddleback tamarins, Leontocebus weddelli (Callitrichidae). In total, 11 compounds of interest (i.e., probably derived from the animals) could be detected in the samples, with 31 of 215 samples containing at least one compound of interest. The composition of these 31 samples varied systematically with species, group, sex, and breeding status. Moreover, we tentatively identified seven of the compounds of interest as methyl hexanoate, benzaldehyde, ethyl hexanoate, acetophenone, a branched C15 alkane, 4-methoxybenzaldehyde, and hexadecan-1-ol. As the field of primate semiochemistry continues to grow, we believe that portable GC-MS instruments have the potential to help make progress in the study of primate chemosignaling in field conditions, despite limitations that we encountered. We further provide recommendations for future use of the Torion® portable GC-MS for in situ analyses.

Rapid evolution of the primate larynx?

Tissue vibrations in the larynx produce most sounds that comprise vocal communication in mammals. Larynx morphology is thus predicted to be a key target for selection, particularly in species with highly developed vocal communication systems. Here, we present a novel database of digitally modeled scanned larynges from 55 different mammalian species, representing a wide range of body sizes in the primate and carnivoran orders. Using phylogenetic comparative methods, we demonstrate that the primate larynx has evolved more rapidly than the carnivoran larynx, resulting in a pattern of larger size and increased deviation from expected allometry with body size. These results imply fundamental differences between primates and carnivorans in the balance of selective forces that constrain larynx size and highlight an evolutionary flexibility in primates that may help explain why we have developed complex and diverse uses of the vocal organ for communication.

Low genetic diversity and limited genetic structure across the range of the critically endangered Mexican howler monkey (Alouatta palliata mexicana).

Genetic diversity provides populations with the possibility to persist in ever-changing environments, where selective regimes change over time. Therefore, the long-term survival of a population may be affected by its level of genetic diversity. The Mexican howler monkey (Alouatta palliata mexicana) is a critically endangered primate restricted to southeast Mexico. Here, we evaluate the genetic diversity and population structure of this subspecies based on 83 individuals from 31 groups sampled across the distribution range of the subspecies, using 29 microsatellite loci. Our results revealed extremely low genetic diversity (HO = 0.21, HE = 0.29) compared to studies of other A. palliata populations and to other Alouatta species. Principal component analysis, a Bayesian clustering method, and analyses of molecular variance did not detect strong signatures of genetic differentiation among geographic populations of this subspecies. Although we detect small but significant FST values between populations, they can be explained by a pattern of isolation by distance. These results and the presence of unique alleles in different populations highlight the importance of implementing conservation efforts in multiple populations across the distribution range of A. p. mexicana to preserve its already low genetic diversity. This is especially important given current levels of population isolation due to the extreme habitat fragmentation across the distribution range of this primate.

Western gorilla space use suggests territoriality.

The evolutionary origins of how modern humans share and use space are often modelled on the territorial-based violence of chimpanzees, with limited comparison to other apes. Gorillas are widely assumed to be non-territorial due to their large home ranges, extensive range overlap, and limited inter-group aggression. Using large-scale camera trapping, we monitored western gorillas in Republic of Congo across 60 km2. Avoidance patterns between groups were consistent with an understanding of the "ownership" of specific regions, with greater avoidance of their neighbours the closer they were to their neighbours' home range centres. Groups also avoided larger groups' home ranges to a greater extent, consistent with stronger defensive responses from more dominant groups. Our results suggest that groups may show territoriality, defending core regions of their home ranges against neighbours, and mirror patterns common across human evolution, with core areas of resident dominance and larger zones of mutual tolerance. This implies western gorillas may be a key system for understanding how humans have evolved the capacity for extreme territorial-based violence and warfare, whilst also engaging in the strong affiliative inter-group relationships necessary for large-scale cooperation.

No evidence that maximum fundamental frequency reflects selection for signal diminution in bonobos.

Acoustic allometry consists of looking at how an organism's body size scales with the characteristics of its vocalizations. A typical finding based on this framework is that across mammals body size is reflected in the fundamental frequency (fo) of vocalizations, whereby lower fo indicates larger body size [1]. This relationship holds owing to the fact that vocal fold length generally scales with body size [2]. Cross-species comparisons allow for the identification of interesting outliers from the body size-f0 regression [3]. Such cases are of particular relevance as they can provide insight into the selective forces potentially driving deviations from standard allometric principles [2]. In a recent study in Current Biology, Grawunder et al.[4] argue that selective pressure for higher f0 has led to the evolution of shorter vocal folds in bonobos than in chimpanzees. Thus, they claim, vocal fold length has evolved independently of body size in bonobos for the purposes of signal diminution (i.e., reducing the impression of body size that they advertise through their calls). However, considering both the existing literature and their own data, this conclusion does not appear to be supported for several reasons.

Fundamental Frequency Estimation of Low-quality Electroglottographic Signals.

Fundamental frequency (fo) is often estimated based on electroglottographic (EGG) signals. Because of the nature of the method, the quality of EGG signals may be impaired by certain features like amplitude or baseline drifts, mains hum, or noise. The potential adverse effects of these factors on fo estimation have to date not been investigated. Here, the performance of 13 algorithms for estimating fo was tested, based on 147 synthesized EGG signals with varying degrees of signal quality deterioration. Algorithm performance was assessed through the standard deviation σfo of the difference between known and estimated fo data, expressed in octaves. With very few exceptions, simulated mains hum, and amplitude and baseline drifts did not influence fo results, even though some algorithms consistently outperformed others. When increasing either cycle-to-cycle fo variation or the degree of subharmonics, the SIGMA algorithm had the best performance (max. σfo = 0.04). That algorithm was, however, more easily disturbed by typical EGG equipment noise, whereas the NDF and Praat's auto-correlation algorithms performed best in this category (σfo = 0.01). These results suggest that the algorithm for fo estimation of EGG signals needs to be selected specifically for each particular data set. Overall, estimated fo data should be interpreted with care.

Neural Correlates of Vocal Repertoire in Primates.

Understanding the nature of the relationship between vocal complexity and brain architecture across non-human primates may help elucidate some of the key elements underlying the evolution of human speech. Here, we report a positive correlation between vocal repertoire size and the relative size of cortical association areas (governing voluntary control over behavioural output) in non-human primates. We further demonstrate that a hominid grade shift in the relative volume of cortical association areas coincides with a similar grade shift in the hypoglossal nucleus (which is associated with the cranial nerve that innervates the muscles of the tongue). Our results support a qualitative continuity in the neural correlates of vocal repertoire, but a quantitative discontinuity in the extent to which the neural system supporting speech is innervated by cortical association areas in great apes and humans.

Publisher Correction: Acoustic allometry revisited: morphological determinants of fundamental frequency in primate vocal production.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has been fixed in the paper.

Publisher Correction: Acoustic allometry revisited: morphological determinants of fundamental frequency in primate vocal production.

A correction to this article has been published and is linked from the HTML version of this paper. The error has not been fixed in the paper.

Acoustic allometry revisited: morphological determinants of fundamental frequency in primate vocal production.

A fundamental issue in the evolution of communication is the degree to which signals convey accurate ("honest") information about the signaler. In bioacoustics, the assumption that fundamental frequency (f o) should correlate with the body size of the caller is widespread, but this belief has been challenged by various studies, possibly because larynx size and body size can vary independently. In the present comparative study, we conducted excised larynx experiments to investigate this hypothesis rigorously and explore the determinants of f o. Using specimens from eleven primate species, we carried out an inter-specific investigation, examining correlations between the minimum f o produced by the sound source, body size and vocal fold length (VFL). We found that, across species, VFL predicted minimum f o much better than body size, clearly demonstrating the potential for decoupling between larynx size and body size in primates. These findings shed new light on the diversity of primate vocalizations and vocal morphology, highlighting the importance of vocal physiology in understanding the evolution of mammal vocal communication.

A demographic history of a population of howler monkeys (Alouatta palliata) living in a fragmented landscape in Mexico.

Long-term field studies are critical for our understanding of animal life history and the processes driving changes in demography. Here, we present long-term demographic data for the northernmost population of mantled howler monkeys (Alouatta palliata) residing in a highly anthropogenically fragmented landscape in Los Tuxtlas, Mexico. We carried out 454 monthly group visits to 10 groups of mantled howler monkeys between 2000 and 2011. The population remained relatively stable over the 11-year study period, with an overall increase in the total number of individuals. Birth rates and inter-birth intervals were comparable to those of howler monkeys at non-fragmented sites, suggesting that living in a fragmented landscape did not affect the reproductive output of our study population. Moreover, despite the landscape, dispersal events were commonplace, including many secondary dispersals (individuals emigrating from groups that they had previously immigrated into). Finally, we found a marked effect of seasonality on the dynamics of our study population. In particular, the period of lowest temperatures and resource scarcity between November and March was associated with higher mortality and reproductive inhibition, while the period of resource abundance between April and May was associated with the majority of conceptions and weaning of offspring. This, in turn, could be influencing dispersal patterns in our study area, as male howler monkeys seem to time some of their immigrations into new groups to coincide with the start of the period of higher fertility, while females preferentially joined new groups several months before the onset of this period. These data have important implications for the conservation and management of howler monkeys in fragmented landscapes, as well as for our understanding of the effect of seasonality over howler monkey dispersal, reproduction and survival.

The coevolution of play and the cortico-cerebellar system in primates.

Primates are some of the most playful animals in the natural world, yet the reason for this remains unclear. One hypothesis posits that primates are so playful because playful activity functions to help develop the sophisticated cognitive and behavioural abilities that they are also renowned for. If this hypothesis were true, then play might be expected to have coevolved with the neural substrates underlying these abilities in primates. Here, we tested this prediction by conducting phylogenetic comparative analyses to determine whether play has coevolved with the cortico-cerebellar system, a neural system known to be involved in complex cognition and the production of complex behaviour. We used phylogenetic generalised least squares analyses to compare the relative volume of the largest constituent parts of the primate cortico-cerebellar system (prefrontal cortex, non-prefrontal heteromodal cortical association areas, and posterior cerebellar hemispheres) to the mean percentage of time budget spent in play by a sample of primate species. Using a second categorical data set on play, we also used phylogenetic analysis of covariance to test for significant differences in the volume of the components of the cortico-cerebellar system among primate species exhibiting one of three different levels of adult-adult social play. Our results suggest that, in general, a positive association exists between the amount of play exhibited and the relative size of the main components of the cortico-cerebellar system in our sample of primate species. Although the explanatory power of this study is limited by the correlational nature of its analyses and by the quantity and quality of the data currently available, this finding nevertheless lends support to the hypothesis that play functions to aid the development of cognitive and behavioural abilities in primates.

Evolutionary trade-off between vocal tract and testes dimensions in howler monkeys.

Males often face a trade-off between investments in precopulatory and postcopulatory traits [1], particularly when male-male contest competition determines access to mates [2]. To date, studies of precopulatory strategies have largely focused on visual ornaments (e.g., coloration) or weapon morphology (e.g., antlers, horns, and canines). However, vocalizations can also play an important role in both male competition and female choice [3-5]. We investigated variation in vocal tract dimensions among male howler monkeys (Alouatta spp.), which produce loud roars using a highly specialized and greatly enlarged hyoid bone and larynx [6]. We examined the relative male investment in hyoids and testes among howler monkey species in relation to the level of male-male competition and analyzed the acoustic consequences of variation in hyoid morphology. Species characterized by single-male groups have large hyoids and small testes, suggesting high levels of vocally mediated competition. Larger hyoids lower formant frequencies, probably increasing the acoustic impression of male body size and playing a role analogous to investment in large body size or weaponry. Across species, as the number of males per group increases, testes volume also increases, indicating higher levels of postcopulatory sperm competition, while hyoid volume decreases. These results provide the first evidence of an evolutionary trade-off between investment in precopulatory vocal characteristics and postcopulatory sperm production.