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.     

Anatomical constraints generate honesty: acoustic cues to age and weight in the roars of red deer stags

Early work on loud calling in mammals emphasized the importance of dynamic characteristics such as calling rate as cues to fitness and fighting ability. In contrast, little is known of the potential for fine-scaled acoustic cues to provide receivers with direct information on fitness. Fundamental frequency has typically been considered a good potential indicator of body size in the literature, but resonance frequencies (formants), which should be constrained by the length of the vocal tract, have received less attention. We conducted a detailed acoustic analysis on an extensive database of roars from red deer stags, Cervus elaphus, in a free-ranging population to investigate which variables provided honest information on age, body weight and reproductive success. Although fundamental frequency was higher in young stags than in adults, it did not decrease with body weight within adults and source cues (i.e. those generated by the larynx) in general did not provide clear information on fitness-related characteristics. In contrast, minimum formant frequencies, reached during the part of the roar when the mobile larynx is most fully retracted towards the sternum, decreased with body weight and age and were strongly negatively correlated with our index of reproductive success. Such production-related acoustic cues to body size and fitness, rendered honest by an anatomical constraint limiting the downward movement of the larynx, provide receivers with accurate information that could be used to assess rivals and choose mates. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Free‐Ranging Red Deer Hinds Show Greater Attentiveness to Roars with Formant Frequencies Typical of Young Males

Acoustic cues present in the reproductive calls of many animal species potentially encode important information about the caller. Here, we test the response of a free‐ranging population of peri‐oestrus red deer hinds to variation in a specific acoustic cue to body size in the male roar, the formant frequencies. Our results revealed: (1) that hinds showed greater overall attention (judged by longer looking responses and lower response latencies) to roars simulating males of sub‐adult body size than to those simulating a large adult male and (2) that hinds without dependent offspring had greater looking responses to male roars and lower response latencies than hinds with dependent offspring to roars simulating sub‐adult males. These findings indicate that free‐ranging red deer hinds may use formants as acoustic cues to gauge the body size and maturity of males in their natural environment, possibly to facilitate earlier detection and avoidance of young stags that are known to harass them.     

Formant Frequencies are Acoustic Cues to Caller Discrimination and are a Weak Indicator of the Body Size of Corncrake Males

Source–filter theory assumes that calls are generated by a vocal source and are subsequently filtered by the vocal tract. The air in the vocal tract vibrates preferentially at certain resonant frequencies, called formants. Formant frequencies can be a good indicator of the caller's characteristics, such as sex, age, body size or individual identity. Although source–filter theory was originally proposed for mammals, formants are also observed in birds, and some bird species have been shown to perceive formants. In this study, we evaluated the hypotheses that formant frequencies (1) are an indicator of body size and (2) can be used for individual discrimination by a nocturnal bird species, the corncrake (Crex crex). We analysed calls of 104 males from Poland and the Czech Republic. Linear regression models showed that the males with a longer head (including the bill length) had a significantly lower formant dispersion and lower fourth and fifth formant frequencies. However, we found no significant relationships between body weight and any filter‐related acoustic measurement. The formant frequencies had smaller within‐ than between‐individual coefficients of variation. This characteristic of the formant frequencies implies a high potential for individual coding. A discriminant function analysis correctly assigned 94.8% of the calls to the caller based on formants from second to fifth. Our results indicated that the formant frequencies are a weak indicator of the body size of the sender in the corncrake. However, even weak dependence between body size and acoustic properties of signal may be important in natural selection process. Alternatively, such a weak dependence may be observed, because receivers ignore the acoustical, formant‐based cues of body size. Simultaneously, the formants might potentially provide acoustic cues to individual discrimination and could be used to census and monitoring tasks.     

Context-related acoustic variation in male fallow deer (Dama dama) groans

While social and behavioural contexts are known to affect the acoustic structure of vocal signals in several mammal species, few studies have investigated context-related acoustic variation during inter-sexual advertisement and/or intra-sexual competition. Here we recorded male fallow deer groans during the breeding season and investigated how key acoustic parameters (fundamental frequency and formant frequencies) vary as a function of the social context in which they are produced. We found that in the presence of females, male fallow deer produced groans with higher mean fundamental frequency when vocal males were also present than they did when no vocal males were in close vicinity. We attribute this to the increased arousal state typically associated with this context. In addition, groan minimum formant frequency spacing was slightly, but significantly lower (indicating marginally more extended vocal tracts) when males were alone than when potential mates and/or competitors were nearby. This indicates that, contrary to our predictions, male fallow deer do not exaggerate the acoustic impression of their body size by further lowering their formant frequencies in the presence of potential mating partners and competitors. Furthermore, since the magnitude of the variation in groan minimum formant frequency spacing remains small compared to documented inter-individual differences, our findings are consistent with the hypothesis that formants are reliable static cues to body size during intra- and inter-sexual advertisement that do not concurrently encode dynamic motivation-related information.     

Red deer stags use formants as assessment cues during intrasexual agonistic interactions

While vocal tract resonances or formants are key acoustic parameters that define differences between phonemes in human speech, little is known about their function in animal communication. Here, we used playback experiments to present red deer stags with re-synthesized vocalizations in which formant frequencies were systematically altered to simulate callers of different body sizes. In response to stimuli where lower formants indicated callers with longer vocal tracts, stags were more attentive, replied with more roars and extended their vocal tracts further in these replies. Our results indicate that mammals other than humans use formants in vital vocal exchanges and can adjust their own formant frequencies in relation to those that they hear.     

Visualizing Sound Emission of Elephant Vocalizations: Evidence for Two Rumble Production Types

Recent comparative data reveal that formant frequencies are cues to body size in animals, due to a close relationship between formant frequency spacing, vocal tract length and overall body size. Accordingly, intriguing morphological adaptations to elongate the vocal tract in order to lower formants occur in several species, with the size exaggeration hypothesis being proposed to justify most of these observations. While the elephant trunk is strongly implicated to account for the low formants of elephant rumbles, it is unknown whether elephants emit these vocalizations exclusively through the trunk, or whether the mouth is also involved in rumble production. In this study we used a sound visualization method (an acoustic camera) to record rumbles of five captive African elephants during spatial separation and subsequent bonding situations. Our results showed that the female elephants in our analysis produced two distinct types of rumble vocalizations based on vocal path differences: a nasally- and an orally-emitted rumble. Interestingly, nasal rumbles predominated during contact calling, whereas oral rumbles were mainly produced in bonding situations. In addition, nasal and oral rumbles varied considerably in their acoustic structure. In particular, the values of the first two formants reflected the estimated lengths of the vocal paths, corresponding to a vocal tract length of around 2 meters for nasal, and around 0.7 meters for oral rumbles. These results suggest that African elephants may be switching vocal paths to actively vary vocal tract length (with considerable variation in formants) according to context, and call for further research investigating the function of formant modulation in elephant vocalizations. Furthermore, by confirming the use of the elephant trunk in long distance rumble production, our findings provide an explanation for the extremely low formants in these calls, and may also indicate that formant lowering functions to increase call propagation distances in this species''.     

Taxonomy and phylogeny of black-and-white colobus monkeys. Inferences from an analysis of loud call variation

Field recordings of male loud calls (or roars) from each major form of black-and-white colobus monkey have been analyzed spectrographically, and features of tempo and pitch measured. Considered together with data on cranial dimensions, coat pattern, and geographical distribution, the results of this analysis suggest that there are five species of black-and-white colobus: Colobus angolensis, C. guereza, C. polykomos, C. satanas, and C. vellerosus. C. guereza and C. vellerosus may have differentiated most recently during a major arid event prior to the last Pleistocene glacial maximum; they have an identical low-pitched roar which we consider to be a shared, derived character. The other species, of which C. satanas has the most distinct roar, may belong to older lineages.     

Arctic roars – laryngeal anatomy and vocalization of the muskox (Ovibos moschatus Zimmermann, 1780, Bovidae)

The impressive roaring of adult male muskoxen most often occurs during rutting contests. Roaring in adult females is primarily relevant to mother–infant communication. Loud roars are produced by taking up a specific roaring posture. Acoustic recordings were made in a small herd of zoo muskoxen during three successive rutting seasons. Earlier recordings of a different herd were used for comparison. Head-and-neck specimens were subjected to vascular injection, macroscopic anatomical dissection, computer tomographic analysis and skeletonization. Isolated preserved larynges of young animals were dissected for ontogenetic comparison. Despite a pronounced sexual dimorphism of head mass, larynx size is almost identical in adult male and female muskoxen, as is the fundamental frequency of their roars. Remarkably, the larynges of both sexes of muskoxen are provided with an unpaired ventrorostral ventricle. Probably, this ventricle is inflated during the initial phase of a roar. The ventricle may have two functions: to increase the amplitude of roaring and to darken the timbre of the roars by acting as an additional resonance space. The vocal fold of adult female and young individuals has a sharp rostral edge and a vocal ligament is still present. During male ontogeny the vocal ligament becomes transformed into a large fat pad extending into the wall of the laryngeal vestibulum. Accordingly, the glottic region in the adult male lacks any sharp edges of the mucosa. In both sexes the thyroarytenoid muscle is divided into three portions. A single roar may comprise phases of different sound volume. The roars of both muskox sexes are characterized by a pulsed structure. We suggest that two oscillating systems are involved in the production of roars: one comprising only the medial portion of the vocal fold and one including its lateral portion.     

Low frequency groans indicate larger and more dominant fallow deer (Dama dama) males

Background

Models of honest advertisement predict that sexually selected calls should signal male quality. In most vertebrates, high quality males have larger body sizes that determine higher social status and in turn higher reproductive success. Previous research has emphasised the importance of vocal tract resonances or formant frequencies of calls as cues to body size in mammals. However, the role of the acoustic features of vocalisations as cues to other quality-related phenotypic characteristics of callers has rarely been investigated.

Methodology/Principal Findings

We examined whether the acoustic structure of fallow deer groans provides reliable information on the quality of the caller, by exploring the relationships between male quality (body size, dominance rank, and mating success) and the frequency components of calls (fundamental frequency, formant frequencies, and formant dispersion). We found that body size was not related to the fundamental frequency of groans, whereas larger males produced groans with lower formant frequencies and lower formant dispersion. Groans of high-ranking males were characterised by lower minimum fundamental frequencies and to a lesser extent, by lower formant dispersions. Dominance rank was the factor most strongly related to mating success, with higher-ranking males having higher mating success. The minimum fundamental frequency and the minimum formant dispersion were indirectly related to male mating success (through dominance rank).

Conclusion/Significance

Our study is the first to show that sexually selected vocalisations can signal social dominance in mammals other than primates, and reveals that independent acoustic components encode accurate information on different phenotypic aspects of male quality.     

Human Vocal Attractiveness as Signaled by Body Size Projection

Voice, as a secondary sexual characteristic, is known to affect the perceived attractiveness of human individuals. But the underlying mechanism of vocal attractiveness has remained unclear. Here, we presented human listeners with acoustically altered natural sentences and fully synthetic sentences with systematically manipulated pitch, formants and voice quality based on a principle of body size projection reported for animal calls and emotional human vocal expressions. The results show that male listeners preferred a female voice that signals a small body size, with relatively high pitch, wide formant dispersion and breathy voice, while female listeners preferred a male voice that signals a large body size with low pitch and narrow formant dispersion. Interestingly, however, male vocal attractiveness was also enhanced by breathiness, which presumably softened the aggressiveness associated with a large body size. These results, together with the additional finding that the same vocal dimensions also affect emotion judgment, indicate that humans still employ a vocal interaction strategy used in animal calls despite the development of complex language.     

Perception of Vocal Tract Resonances by Whooping Cranes Grus americana

Although formants (vocal tract resonances) can often be observed in avian vocalizations, and several bird species have been shown to perceive formants in human speech sounds, no studies have examined formant perception in birds' own species-specific calls. We used playbacks of computer-synthesized crane calls in a modified habituation—dishabituation paradigm to test for formant perception in whooping cranes ( Grus americana ). After habituating birds to recordings of natural contact calls, we played a synthesized replica of one of the habituating stimuli as a control to ensure that the synthesizer worked adequately; birds dishabituated in only one of 13 cases. Then, we played the same call with its formant frequencies shifted. The birds dishabituated to the formant-shifted calls in 10 out of 12 playbacks. These data suggest that cranes perceive and attend to changes in formant frequencies in their own species-specific vocalizations, and are consistent with the hypothesis that formants can provide acoustic cues to individuality and body size.     

Variable asymmetry and resonance in the avian vocal tract: a structural basis for individually distinct vocalizations

The social vocalizations of the oilbird (Steatornis caripensis) frequently have their acoustic energy concentrated into 3 prominent formants which appear to arise from the filter properties of their asymmetrical vocal tract with its bronchial syrinx. The frequency of the second and third formants approximate the predicted fundamental resonances of the unequal left and right cranial portions of each primary bronchus, respectively. Reversibly plugging either bronchus eliminates the corresponding formant. The first formant may arise in the trachea. The degree of vocal tract asymmetry varies between individuals, endowing them with different formant frequencies and providing potential acoustic cues by which individuals of this nocturnal, cave dwelling species may recognize each other in their dark, crowded colonies.     

Do Red Deer Stags (Cervus elaphus) Use Roar Fundamental Frequency (F0) to Assess Rivals?

It is well established that in humans, male voices are disproportionately lower pitched than female voices, and recent studies suggest that this dimorphism in fundamental frequency (F0) results from both intrasexual (male competition) and intersexual (female mate choice) selection for lower pitched voices in men. However, comparative investigations indicate that sexual dimorphism in F0 is not universal in terrestrial mammals. In the highly polygynous and sexually dimorphic Scottish red deer Cervus elaphus scoticus, more successful males give sexually-selected calls (roars) with higher minimum F0s, suggesting that high, rather than low F0s advertise quality in this subspecies. While playback experiments demonstrated that oestrous females prefer higher pitched roars, the potential role of roar F0 in male competition remains untested. Here we examined the response of rutting red deer stags to playbacks of re-synthesized male roars with different median F0s. Our results show that stags’ responses (latencies and durations of attention, vocal and approach responses) were not affected by the F0 of the roar. This suggests that intrasexual selection is unlikely to strongly influence the evolution of roar F0 in Scottish red deer stags, and illustrates how the F0 of terrestrial mammal vocal sexual signals may be subject to different selection pressures across species. Further investigations on species characterized by different F0 profiles are needed to provide a comparative background for evolutionary interpretations of sex differences in mammalian vocalizations.     

Free-Ranging Male Koalas Use Size-Related Variation in Formant Frequencies to Assess Rival Males

Although the use of formant frequencies in nonhuman animal vocal communication systems has received considerable recent interest, only a few studies have examined the importance of these acoustic cues to body size during intra-sexual competition between males. Here we used playback experiments to present free-ranging male koalas with re-synthesised bellow vocalisations in which the formants were shifted to simulate either a large or a small adult male. We found that male looking responses did not differ according to the size variant condition played back. In contrast, male koalas produced longer bellows and spent more time bellowing when they were presented with playbacks simulating larger rivals. In addition, males were significantly slower to respond to this class of playback stimuli than they were to bellows simulating small males. Our results indicate that male koalas invest more effort into their vocal responses when they are presented with bellows that have lower formants indicative of larger rivals, but also show that males are slower to engage in vocal exchanges with larger males that represent more dangerous rivals. By demonstrating that male koalas use formants to assess rivals during the breeding season we have provided evidence that male-male competition constitutes an important selection pressure for broadcasting and attending to size-related formant information in this species. Further empirical studies should investigate the extent to which the use of formants during intra-sexual competition is widespread throughout mammals.     

Nasal and oral calls in mother and young trunk-nosed saiga antelopes,Saiga tatarica

The trunk-like nose of the saiga antelope Saiga tatarica is a striking example of an exaggerated trait, assumed to having evolved as a dust filter for inhaled air. In addition, it functions to elongate the vocal tract in harem saiga males for producing low-formant calls that serve as a cue to body size for conspecifics. This study applies the source–filter theory to the acoustics of nasal, oral and nasal-and-oral calls that were recorded from a captive herd of 24 mother and 32 neonate saigas within the first 10 days postpartum. Anatomical measurements of the nasal and oral vocal tracts of two specimens (one per age class) helped to establish the settings for the analysis of formants. In both mother and young, the lower formants of nasal calls/call parts were in agreement with the source–filter theory, which suggests lower formants for the longer nasal vocal tract than for the shorter oral vocal tract. Similar fundamental frequencies of the nasal and oral parts of nasal-and-oral calls were also in agreement with the source–filter theory, which postulates the independence of source and filter. However, the fundamental frequency was higher in oral than in nasal calls, probably due to the higher emotional arousal during the production of oral calls. We discuss production mechanisms and the ontogeny of formant patterns of oral and nasal calls among bovid and cervid species with and without a trunk-like nose.     

Vocal-tract resonances as indexical cues in rhesus monkeys

Vocal-tract resonances (or formants) are acoustic signatures in the voice and are related to the shape and length of the vocal tract. Formants play an important role in human communication, helping us not only to distinguish several different speech sounds [1], but also to extract important information related to the physical characteristics of the speaker, so-called indexical cues. How did formants come to play such an important role in human vocal communication? One hypothesis suggests that the ancestral role of formant perception--a role that might be present in extant nonhuman primates--was to provide indexical cues [2-5]. Although formants are present in the acoustic structure of vowel-like calls of monkeys [3-8] and implicated in the discrimination of call types [8-10], it is not known whether they use this feature to extract indexical cues. Here, we investigate whether rhesus monkeys can use the formant structure in their "coo" calls to assess the age-related body size of conspecifics. Using a preferential-looking paradigm [11, 12] and synthetic coo calls in which formant structure simulated an adult/large- or juvenile/small-sounding individual, we demonstrate that untrained monkeys attend to formant cues and link large-sounding coos to large faces and small-sounding coos to small faces-in essence, they can, like humans [13], use formants as indicators of age-related body size.     

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.     

Vocal Tract Morphology Determines Species-Specific Features in Vocal Signals of Lemurs (Eulemur)

The source-filter theory describes vocal production as a two-stage process involving the generation of a sound source, with its own spectral structure, which is then filtered by the resonant properties of the vocal tract. This theory has been successfully applied to the study of animal vocal signals since the 1990s. As an extension, models reproducing vocal tract resonance can be used to reproduce formant patterns and to understand the role of vocal tract filtering in nonhuman vocalizations. We studied three congeneric lemur species —Eulemur fulvus, E. macaco, E. rubriventer— using morphological measurements to build computational models of the vocal tract to estimate formants, and acoustic analysis to measure formants from natural calls. We focused on call types emitted through the nose, without apparent articulation. On the basis of anatomical measurements, we modeled the vocal tract of each species as a series of concatenated tubes, with a cross-sectional area that changed along the tract to approximate the morphology of the larynx, the nasopharyngeal cavity, the nasal chambers, and the nostrils. For each species, we calculated the resonance frequencies in 2500 randomly generated vocal tracts, in which we simulated intraspecific length and size variation. Formant location and spacing showed significant species-specific differences determined by the length of the vocal tract. We then measured formants of a set of nasal vocalizations (“grunts”) recorded from captive lemurs of the same species. We found species-specific differences in the natural calls. This is the first evidence that morphology of the vocal tract is relevant in generating filter-related acoustic cues that potentially provide receivers with information about the species of the emitter.     

Vocal and visual attractiveness are related in women

We investigated the relation between visual and vocal attractiveness in women as judged by men. We recorded 34 women speaking four vowels and measured the peak frequency, the first five harmonic frequencies, the first five formant frequencies and formant dispersion. The women were also photographed (head shot), several body measures were taken and their ages were recorded. The voices were played to male judges who were asked to assess the women's age and vocal attractiveness from the recording. The men were then asked to assess the attractiveness of the photographs. Men were in strong agreement on which was an attractive voice and face; and women with attractive faces had attractive voices. Higher-frequency voices were assessed as being more attractive and as belonging to younger women (the lowest frequency produced is a good indicator of age in women in general). Larger women had lower voices and were judged as having less attractive faces and voices. Taller women had narrower formant dispersion as predicted. The results imply that different measures of attractiveness are in agreement and signal similar qualities, such as female age, body size and possibly hormonal profile. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.