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Colonial lagomorphs warn conspecifics of potential danger with alarm calls encoding information about attributes of presumptive predators as well as the caller. In this study, we show that alarm calls of Daurian pikas, Ochotona dauurica (Pallas, 1776), encode information about caller identity. We recorded the alarm calls produced toward a surrogate predator (researcher), slowly moving (0.5–1 km/h) between densely distributed colonies. The alarm calls of most (32 of the 35) callers started in the ultrasonic range at 22.41 kHz on average and rapidly decreased to 3.88 kHz on average at call end. Call duration was very short (0.057 s on average). The accuracy of classifying alarm calls to correct callers with discriminant function analysis (DFA) was 93.71% for the manually measured set of 12 acoustic variables and 95.43% for the semiautomatically measured set of 12 acoustic variables; in both cases exceeding the level of chance (17.28% or 17.33%, respectively). Nonlinear vocal phenomena (biphonations) only were detected in one individual. We discuss the relationship between vocal traits, individuality, vocal production mechanisms, and functions, of pika alarm calls. We propose a potential divergence of alarm calls in Asian pikas to high-frequency whistles (> 20 kHz in Daurian pikas) and in American pikas to low-frequency emissions (0.4–1.3 kHz in Ochotona princeps) during the evolutionary radiation of pikas at the center of the origin of lagomorphs in East Asia and their subsequent geographic dispersal.

A retractable larynx and adaptations of the vocal folds in the males of several polygynous ruminants serve for the production of rutting calls that acoustically announce larger than actual body size to both rival males and potential female mates. Here, such features of the vocal tract and of the sound source are documented in another species. We investigated the vocal anatomy and laryngeal mobility including its acoustical effects during the rutting vocal display of free‐ranging male impala (Aepyceros melampus melampus) in Namibia. Male impala produced bouts of rutting calls (consisting of oral roars and interspersed explosive nasal snorts) in a low‐stretch posture while guarding a rutting territory or harem. For the duration of the roars, male impala retracted the larynx from its high resting position to a low mid‐neck position involving an extensible pharynx and a resilient connection between the hyoid apparatus and the larynx. Maximal larynx retraction was 108 mm based on estimates in video single frames. This was in good concordance with 91‐mm vocal tract elongation calculated on the basis of differences in formant dispersion between roar portions produced with the larynx still ascended and those produced with maximally retracted larynx. Judged by their morphological traits, the larynx‐retracting muscles of male impala are homologous to those of other larynx‐retracting ruminants. In contrast, the large and massive vocal keels are evolutionary novelties arising by fusion and linear arrangement of the arytenoid cartilage and the canonical vocal fold. These bulky and histologically complex vocal keels produced a low fundamental frequency of 50 Hz. Impala is another ruminant species in which the males are capable of larynx retraction. In addition, male impala vocal folds are spectacularly specialized compared with domestic bovids, allowing the production of impressive, low‐frequency roaring vocalizations as a significant part of their rutting behaviour. Our study expands knowledge on the evolutionary variation of vocal fold morphology in mammals, suggesting that the structure of the mammalian sound source is not always human‐like and should be considered in acoustic analysis and modelling., Male impala retract the larynx while producing their impressive rutting roars. The low fundamental frequency of these roars is produced by a highly modified vocal fold, a ‘vocal keel’. The anatomical and acoustical correlates of male impala's mobile larynx are discussed.

Eurasian deer are characterized by the extraordinary diversity of their vocal repertoires. Male sexual calls range from roars with relatively low fundamental frequency (hereafter f o) in red deer Cervus elaphus, to moans with extremely high f o in sika deer Cervus nippon, and almost infrasonic groans with exceptionally low f o in fallow deer Dama dama. Moreover, while both red and fallow males are capable of lowering their formant frequencies during their calls, sika males appear to lack this ability. Female contact calls are also characterized by relatively less pronounced, yet strong interspecific differences. The aim of this study is to examine the anatomical bases of these inter‐specific and inter‐sexual differences by identifying if the acoustic variation is reflected in corresponding anatomical variation. To do this, we investigated the vocal anatomy of male and female specimens of each of these three species. Across species and sexes, we find that the observed acoustic variability is indeed related to expected corresponding anatomical differences, based on the source‐filter theory of vocal production. At the source level, low f o is associated with larger vocal folds, whereas high f o is associated with smaller vocal folds: sika deer have the smallest vocal folds and male fallow deer the largest. Red and sika deer vocal folds do not appear to be sexually dimorphic, while fallow deer exhibit strong sexual dimorphism (after correcting for body size differences). At the filter level, the variability in formants is related to the configuration of the vocal tract: in fallow and red deer, both sexes have evolved a permanently descended larynx (with a resting position of the larynx much lower in males than in females). Both sexes also have the potential for momentary, call‐synchronous vocal tract elongation, again more pronounced in males than in females. In contrast, the resting position of the larynx is high in both sexes of sika deer and the potential for further active vocal tract elongation is virtually absent in both sexes. Anatomical evidence suggests an evolutionary reversal in larynx position within sika deer, that is, a secondary larynx ascent. Together, our observations confirm that the observed diversity of vocal behaviour in polygynous deer is supported by strong anatomical differences, highlighting the importance of anatomical specializations in shaping mammalian vocal repertoires. Sexual selection is discussed as a potential evolutionary driver of the observed vocal diversity and sexual dimorphisms., The comparison of three species of acoustically diverse polygynous deer suggests that acoustic variability is related to corresponding anatomical differences of the vocal organs.

The acoustics of male rutting roars, aside from genetic markers, are useful tools for characterization of populations and subspecies of red deer Cervus elaphus. This study of rutting mature male Pannonian red deer from Southern Hungary presents a description of the calling posture, a graphical reconstruction of the oral vocal tract length during rutting roar production and a spectrographic analyses of 1740 bouts containing a total of 5535 rutting roars. In addition, this study provides the first direct comparison of the bouts and main (=longest) rutting roars between Pannonian and Iberian red deer stags, representative of the Western and Eastern lineages of European red deer. The bouts of the Pannonian stags comprised 1–15 roars per bout; 24.37% were single-roar bouts and 23.68% were two-roar bouts. The duration of the main roars within bouts ranged from 0.52s to 4.60s, 1.13±0.50s on average. Main common roars (66.3% of the 1740 main roars), were longer than harsh roars (1.27±0.55s vs 0.87±0.25s) and higher in maximum fundamental frequency (179 ± 61 Hz vs 147 ± 54 Hz). In multi-roar bouts, main harsh roars were first roars in 47.4%, intermediate roars in 19.2% and last roars in 18.8% of the bouts. Bout structure and the acoustics of main roars in the Pannonian stags differed from those in the Iberian stags and in stags from other populations of Cervus elaphus. These results support the power of rutting vocalizations for consideration as an additional tool for discriminating populations and subspecies within Cervus elaphus.

BackgroundThe rutting vocal display of male impalaAepyceros melampusis unique for its complexity among ruminants. This study investigates bouts of rutting calls produced towards potential mates and rival males by free-ranging male impala in Namibia. In particular, a comparison of male rutting and alarm snorts is conducted, inspired by earlier findings of mate guarding by using alarm snorts in male topiDamaliscus lunatus.ResultsRutting male impala produced 4–38 (13.5 ± 6.5) rutting calls per bout. We analyzed 201 bouts, containing in total 2709 rutting calls of five types: continuous roars produced within a single exhalation-inhalation cycle; interrupted roars including few exhalation-inhalation cycles; pant-roars distinctive by a pant-phase with rapidly alternating inhalations and exhalations; usual snorts lacking any roar part; and roar-snorts starting with a short roar part. Bouts mostly started and ended with usual snorts. Continuous roars were the shortest roars. The average duration of the exhalatory phase was longest in the continuous roars and shortest in the pant-roars. The average fundamental frequency (49.7–51.4 Hz) did not differ between roar types. Vocal tract length, calculated by using measurements of the first four vocal tract resonances (formants), ranged within 381–382 mm in all roar types. In the studied male impala, rutting snorts within bouts of rutting calls were longer and had higher values of the upper quartile in the call spectra than alarm snorts produced towards potential danger.ConclusionsAdditional inhalations during the emission of the interrupted and pant-roars prolong their duration compared to the continuous roars but do not affect the fundamental frequency or the degree of larynx retraction while roaring. Alarm snorts are separated from one another by large intervals, whereas the intervals between rutting snorts within bouts are short. Sometimes, rutting snorts alternate with roars, whereas alarm snorts do not. Therefore, it is not the acoustic structure of individual snorts but the temporal sequence and the occasional association with another call type that defines snorts as either rutting or alarm snorts. The rutting snorts of male impala may function to attract the attention of receptive females and delay their departure from a male’s harem or territory.

Koalas are characterised by a highly unusual vocal anatomy, with a descended larynx and velar vocal folds, allowing them to produce calls with disproportionately low frequencies. Here we use advanced imaging techniques, histological data, classical macroscopic dissection and behavioural observations to provide the first detailed description and interpretation of male and female koala vocal anatomy. We show that both males and females have an elongated pharynx and soft palate, resulting in a permanently descended larynx. In addition, the hyoid apparatus has a human-like configuration in which paired dorsal, resilient ligaments suspend the hyoid apparatus from the skull, while the ventral parts tightly connect to the descended larynx. We also show that koalas can retract the larynx down into the thoracic inlet, facilitated by a dramatic evolutionary transformation of the ventral neck muscles. First, the usual retractors of the larynx and the hyoid have their origins deep in the thorax. Second, three hyoid muscles have lost their connection to the hyoid skeleton. Third, the genioglossus and geniohyoid muscles have greatly increased in length. Finally, the digastric, omohyoid and sternohyoid muscles, connected by a common tendinous intersection, form a guiding channel for the dynamic down-and-up movements of the ventral hyoid parts and the larynx. We suggest that these features evolved to accommodate the low resting position of the larynx and assist in its retraction during call production. We also confirm that the edges of the intra-pharyngeal ostium have specialised to form the novel, extra-laryngeal velar vocal folds, which are much larger than the true, intra-laryngeal vocal folds in both sexes, but more developed and specialised for low frequency sound production in males than in females. Our findings illustrate that strong selection pressures on acoustic signalling not only lead to the specialisation of existing vocal organs, but can also result in the evolution of novel vocal structures in both sexes.

Neonate ruminants produce distress calls when captured by a predator and discomfort milk begging calls when hungry. In many neonate ruminants, the distress and discomfort calls are high-frequency vocalizations, in which the fundamental frequency is the key variable for recognition of their emotional arousal by caregivers. In contrast, in this study, we examine the low-frequency open-mouth distress and discomfort calls in the neonates of two species of wild-living ungulates, which clearly highlight vocal tract resonances (formants). In the goitred gazelle (Gazella subgutturosa), the distress calls were higher in fundamental frequency (f0) and in the first and third formants than the discomfort calls. The accuracy of classifying individuals by variables of distress calls with discriminant function analysis (67%) was significantly lower than that of discomfort calls (85%). In the saiga (Saiga tatarica), only the third formant was higher in the distress calls than in the discomfort calls. The accuracy of classifying individuals by variables of distress calls (89%) did not differ significantly from that of discomfort calls (94%). Thus, the use of acoustic cues to vocal identity and to the degree of arousal differs between the two species. Calls were significantly more individualistic in the saiga, probably because this species lives in large herds and neonates use a ‘following’ antipredatory strategy, in which vocal individuality is crucial for mother–offspring communication. In contrast, goitred gazelles live in smaller groups and neonates use a ‘hiding’ antipredatory strategy. Accordingly, mothers can rely on additional environmental cues for spotting their young and this may decrease the necessity for individualization of the calls of neonates.

The pronouncedly enlarged and descended larynx in male goitred gazelles (Gazella subgutturosa), Mongolian gazelles (Procapra gutturosa) and fallow deer (Dama dama) represents an interesting parallel to the 'Adam's apple' of human males. Goitred gazelles, as humans, are not born with a descended larynx. Therefore the sexual dimorphism of larynx size and position develops during ontogeny. In this study, the vocal ontogeny of male and female goitred gazelles was investigated across five age classes from neonates to adults. The acoustic variables of nasal contact calls were measured in 53 (24 male, 29 female) individuals, body mass and neck dimensions in 63 (31 male, 32 female) live individuals and nasal vocal tract and vocal fold lengths in 26 (16 male, 10 female) anatomical specimens. Call fundamental frequency (f0), the acoustic correlate of the ontogenetically enlarging larynx, decreased significantly in either sex. Call formants (second, third and forth), the acoustic correlates of the ontogenetically elongating vocal tract, did not differ significantly between sexes up to early adulthood, but clearly diverged in adults. Significant differences between sexes in neck circumference at the level of the larynx emerged already at 2-3 months of age, whereas body mass, neck circumference at the neck-body transition and the degree of larynx descent significantly differed in adults only. We discuss that, in contrast to humans, the accelerated enlargement of the larynx in male goitred gazelles starts early in ontogeny. A moderate descent of the larynx develops equally in both sexes before early adulthood, whereas the additional prominent descent of the larynx in males is shifted to late ontogeny. This might avoid selective disadvantages of this sexually dimorphic trait on males during their period of growth. As has been previously proved for humans, the emergence of the strong male-specific descent of the larynx in goitred gazelles may go along with the increasing social status and the males' increasing chances of siring offspring. Similar to the Adam's apple of human males, this may indicate the important role of the enlarged and descended larynx for signaling male status via masculine voice.

Whereas low-frequency bellows (below 200 Hz) have been investigated in detail in both male and female domestic cattle (Bos taurus), male high-frequency bugle calls (over 800 Hz) have not been described so far in any large bovid species. In this study, high-frequency bugles and low-frequency bellows were recorded from three crossbred free-ranging domestic cattle bulls and analysed spectrographically. The maximum fundamental frequency of bellows was 113.6 Hz, whereas the maximum fundamental frequency of bugles was 958.4 Hz, ranging from 801 to 1125 Hz in different males. These amazingly high fundamental frequencies of bull bugles are comparable with those reported for Siberian wapiti Cervus elaphus sibiricus, but lower than reported values for some subspecies of North American wapiti Cervus canadensis. The similarity with both Siberian and North American wapiti was also observed in the production of bull biphonic bugles with two fundamental frequencies: the low and the high one. We suggest that bugl...

This study quantitatively documents the progressive development of sexual dimorphism of the vocal organs along the ontogeny of the goitred gazelle (Gazella subgutturosa). The major, male-specific secondary sexual features, of vocal anatomy in goitred gazelle are an enlarged larynx and a marked laryngeal descent. These features appear to have evolved by sexual selection and may serve as a model for similar events in male humans. Sexual dimorphism of larynx size and larynx position in adult goitred gazelles is more pronounced than in humans, whereas the vocal anatomy of neonate goitred gazelles does not differ between sexes. This study examines the vocal anatomy of 19 (11 male, 8 female) goitred gazelle specimens across three age-classes, that is, neonates, subadults and mature adults. The postnatal ontogenetic development of the vocal organs up to their respective end states takes considerably longer in males than in females. Both sexes share the same features of vocal morphology but differences emerge in the course of ontogeny, ultimately resulting in the pronounced sexual dimorphism of the vocal apparatus in adults. The main differences comprise larynx size, vocal fold length, vocal tract length, and mobility of the larynx. The resilience of the thyrohyoid ligament and the pharynx, including the soft palate, and the length changes during contraction and relaxation of the extrinsic laryngeal muscles play a decisive role in the mobility of the larynx in both sexes but to substantially different degrees in adult females and males. Goitred gazelles are born with an undescended larynx and, therefore, larynx descent has to develop in the course of ontogeny. This might result from a trade-off between natural selection and sexual selection requiring a temporal separation of different laryngeal functions at birth and shortly after from those later in life. J. Morphol. 277:826-844, 2016. © 2016 Wiley Periodicals, Inc.

International audience; Males of several species of deer have a descended and mobile larynx, resulting in an unusually long vocal tract, which can be further extended by lowering the larynx during call production. Formant frequencies are lowered as the vocal tract is extended, as predicted when approximating the vocal tract as a uniform quarter wavelength resonator. However, formant frequencies in polygynous deer follow uneven distribution patterns, indicating that the vocal tract configuration may in fact be rather complex. We CT-scanned the head and neck region of two adultmale fallowdeer specimens with artificially extended vocal tracts and measured the cross-sectional areas of the supralaryngeal vocal tract along the oral and nasal tracts. The CT data were then used to predict the resonances produced by three possible configurations, including the oral vocal tract only, the nasal vocal tract only, or combining the two. We found that the area functions from the combined oral and nasal vocal tracts produced resonances more closely matching the formant pattern and scaling observed in fallow deer groans than those predicted by the area functions of the oral vocal tract only or of the nasal vocal tract only. This indicates that the nasal and oral vocal tracts are both simultaneously involved in the production of a non-human mammal vocalization, and suggests that the potential for nasalization in putative oral loud calls should be carefully considered.

The ability of adult and subadult piebald shrews ( Diplomesodon pulchellum ) to produce 160 Hz seismic waves is potentially reflected in their vocal ontogeny and ear morphology. In this study, the ontogeny of call variables and body traits was examined in 11 litters of piebald shrews, in two-day intervals from birth to 22 days (subadult), and ear structure was investigated in two specimens using micro-computed tomography (micro-CT). Across ages, the call fundamental frequency (f0) was stable in squeaks and clicks and increased steadily in screeches, representing an unusual, non-descending ontogenetic pathway of f0. The rate of the deep sinusoidal modulation (pulse rate) of screeches increased from 75 Hz at 3–4 days to 138 Hz at 21–22 days, probably relating to ontogenetic changes in contraction rates of the same muscles which are responsible for generating seismic vibrations. The ear reconstructions revealed that the morphologies of the middle and inner ears of the piebald shrew are very similar to those of the common shrew ( Sorex araneus ) and the lesser white-toothed shrew ( Crocidura suaveolens ), which are not known to produce seismic signals. These results suggest that piebald shrews use a mechanism other than hearing for perceiving seismic vibrations.

In neonate ruminants, the acoustic structure of vocalizations may depend on sex, vocal anatomy, hormonal profiles and body mass and on environmental factors. In neonate wild-living Mongolian gazelles Procapra gutturosa, hand-captured during biomedical monitoring in the Daurian steppes at the Russian-Mongolian border, we spectrographically analysed distress calls and measured body mass of 22 individuals (6 males, 16 females). For 20 (5 male, 15 female) of these individuals, serum testosterone levels were also analysed. In addition, we measured relevant dimensions of the vocal apparatus (larynx, vocal folds, vocal tract) in one stillborn male Mongolian gazelle specimen. Neonate distress calls of either sex were high in maximum fundamental frequency (800–900 Hz), but the beginning and minimum fundamental frequencies were significantly lower in males than in females. Body mass was larger in males than in females. The levels of serum testosterone were marginally higher in males. No correlations were found between either body mass or serum testosterone values and any acoustic variable for males and females analysed together or separately. We discuss that the high-frequency calls of neonate Mongolian gazelles are more typical for closed-habitat neonate ruminants, whereas other open-habitat neonate ruminants (goitred gazelle Gazella subgutturosa, saiga antelope Saiga tatarica and reindeer Rangifer tarandus) produce low-frequency (

Saiga antelopes Saiga tatarica tatarica give birth in large aggregations, and offspring follow the herd soon after birth. Herding is advantageous as anti-predator strategy; however, communication between mothers and neonates is strongly complicated in large aggregations. Individual series of nasal and oral contact calls of mother and neonate saiga antelopes were selected from recordings made with automated recording systems placed near the hiding neonates on the saiga breeding grounds in Northern Kazakhstan during synchronized parturitions of 30,000 calving females. We used for comparison of the acoustic structure of nasal and oral contact calls 168 nasal calls of 18 mothers, 192 oral calls of 21 mothers, 78 nasal calls of 16 neonates, and 197 oral calls of 22 neonates. In the oral calls of either mothers or neonates, formant frequencies were higher and the duration was longer than in the nasal calls, whereas fundamental frequencies did not differ between oral and nasal calls. Discriminant function analysis (DFA) based on six acoustic variables, accurately classified individual identity for 99.4% of oral calls of 18 mothers, for 89.3% of nasal calls of 18 mothers, and for 94.4% of oral calls of 18 neonates. The average value of correct classification to individual was higher in mother oral than in mother nasal calls and in mother oral calls than in neonate oral calls; no significant difference was observed between mother nasal and neonate oral calls. Variables mainly responsible for vocal identity were the fundamental frequency and the second and third formants in either mothers or neonates, and in either nasal or oral calls. The high vocal identity of mothers and neonates suggests a powerful potential for the mutual mother-offspring recognition in dense aggregations of saiga antelopes as an important component of their survival strategy.

SUMMARYElephants' low-frequency vocalizations are produced by flow-induced self-sustaining oscillations of laryngeal tissue. To date, little is known in detail about the vibratory phenomena in the elephant larynx. Here, we provide a first descriptive report of the complex oscillatory features found in the excised larynx of a 25 year old female African elephant (Loxodonta africana), the largest animal sound generator ever studied experimentally. Sound production was documented with high-speed video, acoustic measurements, air flow and sound pressure level recordings. The anatomy of the larynx was studied with computed tomography (CT) and dissections. Elephant CT vocal anatomy data were further compared with the anatomy of an adult human male. We observed numerous unusual phenomena, not typically reported in human vocal fold vibrations. Phase delays along both the inferior–superior and anterior–posterior (A–P) dimension were commonly observed, as well as transverse travelling wave patterns along the A–P dimension, previously not documented in the literature. Acoustic energy was mainly created during the instant of glottal opening. The vestibular folds, when adducted, participated in tissue vibration, effectively increasing the generated sound pressure level by 12 dB. The complexity of the observed phenomena is partly attributed to the distinct laryngeal anatomy of the elephant larynx, which is not simply a large-scale version of its human counterpart. Travelling waves may be facilitated by low fundamental frequencies and increased vocal fold tension. A travelling wave model is proposed, to account for three types of phenomena: A–P travelling waves, ‘conventional’ standing wave patterns, and irregular vocal fold vibration.

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 agreemen...

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.

With an average male body mass of 320 kg, the wapiti, Cervus canadensis, is the largest extant species of Old World deer (Cervinae). Despite this large body size, male wapiti produce whistle-like sexual calls called bugles characterised by an extremely high fundamental frequency. Investigations of the biometry and physiology of the male wapiti's relatively large larynx have so far failed to account for the production of such a high fundamental frequency. Our examination of spectrograms of male bugles suggested that the complex harmonic structure is best explained by a dual-source model (biphonation), with one source oscillating at a mean of 145 Hz (F0) and the other oscillating independently at an average of 1426 Hz (G0). A combination of anatomical investigations and acoustical modelling indicated that the F0 of male bugles is consistent with the vocal fold dimensions reported in this species, whereas the secondary, much higher source at G0 is more consistent with an aerodynamic whistle produced as air flows rapidly through a narrow supraglottic constriction. We also report a possible interaction between the higher frequency G0 and vocal tract resonances, as G0 transiently locks onto individual formants as the vocal tract is extended. We speculate that male wapiti have evolved such a dual-source phonation to advertise body size at close range (with a relatively low-frequency F0 providing a dense spectrum to highlight size-related information contained in formants) while simultaneously advertising their presence over greater distances using the very high-amplitude G0 whistle component.

Source–filter coupling is the rarest acoustic phenomenon not only in Iberian red deer, but in any mammal. In most mammals, sound production can be well described in the framework of source–filter theory. The vocal output is the result of combined work of the larynx (the source) and of the supralaryngeal vocal tract (the filter). The source–filter theory suggests the independence of source and filter. Thus, vocal tract filtering should not affect the fundamental frequency (f0) of the sound created in the larynx. Spectrographically, the source is mostly characterized by the f0 and its harmonics, while the filter by the vocal tract resonances, i.e., formant frequencies. Nevertheless, a non-independent (coupled) source and filter can be proposed when the vocal folds start oscillating at one of the formant frequencies. Coupling between source and filter has been found in human singers and predicted for red deer Cervus elaphus by a computer modeling approach. This study describes different modes of phonation in a natural bout of rutting calls of Iberian red deer Cervus elaphus hispanicus and the transition from a chaotic mode to a probable source–filter coupling mode. This phenomenon might be involved in the production of extremely high-frequency bugles of North American and Asian subspecies of C. elaphus.

Individualistic voices are important for establishing personalized relationships among individuals. In young animals, individual vocal identity is affected by permanent changes of the acoustics due to the growth of their vocal apparatus. Different acoustic variables change uncoordinatedly, so vocal individuality should be repeatedly upgraded along development. We compared classifying accuracy of individuals and sexes by nasal calls in fast-growing goitred gazelles Gazella subgutturosa at two ontogenetic stages, juvenile (3-6 weeks of age) and adolescent (23-26 weeks of age). Juvenile "spring" nasal calls and adolescent "fall" nasal calls were examined in the same 35 calves (18 males, 17 females), wild-born in May and then hand-raised. Discriminate function analysis based on four formants, fundamental frequency, duration and three power quartiles, revealed an equally high potential of spring and fall calls to encode sex. The individuality was very high in both ages but significantly higher in fall calls. Classifying calls to individuals was based on the same three acoustic variables (fundamental frequency and third and fourth formants) in both ages, although their actual values changed uncoordinatedly from spring to fall in most subjects. Our results suggest updating acoustic individuality in nasal calls of adolescent goitred gazelles accordingly to the newly emerged acoustic variation.

Roaring in rutting Iberian red deer stags Cervus elaphus hispanicus is unusual compared to other subspecies of red deer, which radiated from the Iberian refugium after the last glacial maximum. In all red deer stags, the larynx occupies a permanent low mid-neck resting position and is momentarily retracted almost down to the rostral end of the sternum during the production of rutting calls. Simultaneous with the retraction of the larynx, male Iberian red deer pronouncedly protrude the tongue during most of their rutting roars. This poses a mechanical challenge for the vocal tract (vt) and for the hyoid apparatus, as tongue and larynx are strongly pulled in opposite directions. This study (i) examines the vocal anatomy and the acoustics of the rutting roars in free-ranging male C. e. hispanicus; (ii) establishes a potential mechanism of simultaneous tongue protrusion and larynx retraction by applying a two-dimensional model based on graphic reconstructions in single video frames of unrestrained animals; and (iii) advances a hypothesis of evaporative cooling by tongue protrusion in the males of a subspecies of red deer constrained to perform all of the exhausting rutting activities, including acoustic display, in a hot and arid season.

This study quantitatively documents the progressive development of sexual dimorphism of the vocal organs along the ontogeny of the goitred gazelle (Gazella subgutturosa). The major, male-specific secondary sexual features, of vocal anatomy in goitred gazelle are an enlarged larynx and a marked laryngeal descent. These features appear to have evolved by sexual selection and may serve as a model for similar events in male humans. Sexual dimorphism of larynx size and larynx position in adult goitred gazelles is more pronounced than in humans, whereas the vocal anatomy of neonate goitred gazelles does not differ between sexes. This study examines the vocal anatomy of 19 (11 male, 8 female) goitred gazelle specimens across three age-classes, that is, neonates, subadults and mature adults. The postnatal ontogenetic development of the vocal organs up to their respective end states takes considerably longer in males than in females. Both sexes share the same features of vocal morphology but differences emerge in the course of ontogeny, ultimately resulting in the pronounced sexual dimorphism of the vocal apparatus in adults. The main differences comprise larynx size, vocal fold length, vocal tract length, and mobility of the larynx. The resilience of the thyrohyoid ligament and the pharynx, including the soft palate, and the length changes during contraction and relaxation of the extrinsic laryngeal muscles play a decisive role in the mobility of the larynx in both sexes but to substantially different degrees in adult females and males. Goitred gazelles are born with an undescended larynx and, therefore, larynx descent has to develop in the course of ontogeny. This might result from a trade-off between natural selection and sexual selection requiring a temporal separation of different laryngeal functions at birth and shortly after from those later in life. J. Morphol. 277:826-844, 2016. © 2016 Wiley Periodicals, Inc.

Similar to male humans, Homo sapiens, the males of a few polygynous ruminants – red deer Cervus elaphus, fallow deer Dama dama and Mongolian gazelle Procapra gutturosa– have a more or less enlarged, low-resting larynx and are capable of additional dynamic vocal tract elongation by larynx retraction during their rutting calls. The vocal correlates of a large larynx and an elongated vocal tract, a low fundamental frequency and low vocal tract resonance frequencies, deter rival males and attract receptive females. The males of the polygynous goitred gazelle, Gazella subgutturosa, provide another, independently evolved, example of an enlarged and low-resting larynx of high mobility. Relevant aspects of the rutting behaviour of territorial wild male goitred gazelles are described. Video and audio recordings served to study the acoustic effects of the enlarged larynx and vocal tract elongation on male rutting calls. Three call types were discriminated: roars, growls and grunts. In addition, the adult male vocal anatomy during the emission of rutting calls is described and functionally discussed using a 2D-model of larynx retraction. The combined morphological, behavioural and acoustic data are discussed in relation to the hypothesis of sexual selection for male-specific deep voices, resulting in convergent features of vocal anatomy in a few polygynous ruminants and in human males.

Like many other gazelles, goitred gazelles (Gazella subgutturosa) are capable of calling either through the nose or through the open mouth. In particular, juvenile goitred gazelles provide a convenient model for contrasting acoustic characteristics of nasal and oral calls, and for estimating their communicative functions. In this study, acoustic variables (formants, fundamental frequency, duration and power quartiles) of 480 oral and 483 nasal calls, recorded from 20 (9 male, 11 female) individually identified captive juvenile goitred gazelles, were examined for their potential to encode sex and identity of the caller. Discriminant function analysis revealed an equally high potential of oral and nasal calls to encode sex, whereas encoding the individual identity was significantly more accurate for oral calls. Sex was encoded exclusively in formants, whilst individual identity was encoded in a combination of all investigated variables. No correlation was found between body mass and values of any acoustic variable. Analyses controlling for age and sex revealed higher average values for all investigated variables of oral calls compared to nasal calls. We discuss the results in relation to the sourcefilter theory, mother–offspring communication and production mechanisms of nasal and oral calls in mammals.

This study provides the first evidence of pronounced temporary laryngeal descent in a bovid species. An elaborate acoustic display is prominent in male courtship behavior of polygynous Mongolian gazelle. During rut, rounding up of females is accompanied by continuous head-up barking by dominant males. Throughout the rut their evolutionarily enlarged larynx descends to a low mid-neck resting position. In the course of each bark the larynx is additionally retracted toward the sternum by 30% of the resting vocal tract length. A geometric model of active larynx movements was constructed by combining results of video documentation, dissection, skeletonization, and behavioral observation. The considerable distance between resting position and maximal laryngeal descent suggests a backward tilting of the hyoid apparatus and an extension of the thyrohyoid connection during the retraction phase. Return to the resting position is effected by strap muscles and by the elastic recoil of the pharynx and the thyrohyoid connection. An intrapharyngeal inflation of the peculiar palatinal pharyngeal pouch of adult males is inferred from a short-time expansion of the ventral neck region rostral to the laryngeal prominence. The neck of adult dominant males is accentuated by long gray guard hairs during the rut. The passive swinging of the heavy larynx of adult males during locomotion gives the impression of a handicap imposed on rutting males. Apparently, this disadvantage becomes outweighed by the profits for reproductive success. J. Morphol., 2008. © 2008 Wiley-Liss, Inc.

Biphonation, i.e. two independent fundamental frequencies in a call spectrum, is a prominent feature of vocal activity in dog-like canids. Dog-like canids can produce a low (f0) and a high (g0) fundamental frequency simultaneously. In contrast, fox-like canids are only capable of producing the low fundamental frequency (f0). Using a comparative anatomical approach for revealing macroscopic structures potentially responsible for canid biphonation, we investigated the vocal anatomy for 4 (1 male, 3 female) captive dholes (Cuon alpinus) and for 2 (1 male, 1 female) wild red fox (Vulpes vulpes). In addition, we analyzed the acoustic structure of vocalizations in the same dholes that served postmortem as specimens for the anatomical investigation. All study dholes produced both high-frequency and biphonic calls. The anatomical reconstructions revealed that the vocal morphologies of the dhole are very similar to those of the red fox. These results suggest that the high-frequency and biphonic calls in dog-like canids can be produced without specific anatomical adaptations of the sound-producing structures. We discuss possible production modes for the high-frequency and biphonic calls involving laryngeal and nasal structures.

In most mammals the larynx has a high resting position close to the root of the tongue. An exception to this are humans with a descended larynx. Some other species of mammals convergently evolved a...

Males of several species of deer have a descended larynx, which gives them an unusually long vocal tract (VT). They can extend their VT by further lowering their larynx during the production of their sexual loudcalls. Formant frequencies are lowered as the vocal tract is extended, as predicted when approximating the vocal tract as a uniform quarter wavelength resonator. However, formant frequencies in polygynous deer follow uneven distribution patterns, suggesting that the vocal tract shape is in fact rather complex. We CT-scanned the artificially extended vocal tract of two adult fallow deer, and measured the cross-sectional area of the supralyngeal vocal tract along the oral and nasal pathways. We used this data to model resonances patterns produced by these VT including the oral pathway, the nasal pathway, or both. We found that the combined oral/nasal VT produced a formant pattern that more closely matches that observed in fallow deer groans and enables a better estimation of VT length from formant pa...

The larynges (except for the epiglottis) of two adult Mongolian gazelles, one male and one female, were dis- sected. This species is characterized by a pronounced sexual dimorphism of the larynx. Dimorphism with regard to the size of the entire larynx and of the thyroid cartilage is about 2:1 whereas the difference of mean body mass is about 1.3:1 between males and females. Unexpectedly, and in contrast to other bovids, the larynx of the male Mongolian gazelle has a paired lateral laryngeal ventricle. However, in contrast to horse, dog, pig and many primate species also possessing such a paired ventricle, its rostral opening in the Mongolian gazelle is situated lateral to the corniculate pro- cess of the arytenoid cartilage. The neck of the laryngeal ventricle is embraced by the bifurcated cuneiform process of the epiglottis. Despite the enlarged laryngeal cartilages, the vocal process of the male arytenoid cartilage is relatively shorter than that of the female. The male thyroarytenoid muscle is clearly separated into a rostral ventricular muscle and a caudal vocal muscle whereas the female's, as in other bovids, is almost uniform. The lateral sac of the two-cham- bered laryngeal ventricle in the male projects laterally between the ventricular and the vocal muscle. As in the domestic bovids and in many other artiodactyls the larynx of the male Mongolian gazelle is lacking any rostrally directed mem- braneous portion of the vocal fold. Instead, the thick and tough bow-like vocal fold projects caudally into the infraglot- tic cavity and is supported by a peculiar pan-like fibroelastic pad. This resilient element, situated medial to the bipartite thyroarytenoid muscle, might be a homologue of the vocal ligament, eventually including lateral portions of the elastic cone. A fibroelastic pad is absent in the female. The resilient floor of the laryngeal vestibulum, ventral to the fibroelas- tic pad, is rostrally and caudally subducted by tube-like spaces. Evolutionary enlargement of the male larynx, including the vocal folds, and of the caudal portions of the vocal tract may have shifted the fundamental and formant frequencies to a lower register. The paired lateral laryngeal ventricle might produce an amplitude increase of the vocalizations assisted by differential action of the bipartite thyroarytenoid muscle. In addition, the peculiar shape, size and tough consistency of the male vocal folds may, as in roaring felids, assist in producing high amplitude and low frequency vocalizations. Perhaps the biological role of the enlarged male larynx of Procapra gutturosahas evolved in relation to its mating system. In the rutting season, dominant males establish individual territories and maintain harems. During prolonged courtship prior to mating, these males perform an acoustic display uttering loud and guttural bellows. In addition, the bulging ventral neck region of males may serve as an optical attractant for the females. Thus, the evolution of the enlarged larynx of the male Mongolian gazelle may have been favoured by sexual selection.

A five and a half weeks old female Kestrel exhibiting osteopathy of the pectoral and pelvic limbs, including symmetrical hyperdactyly, was investigated in order to clarify the pattern of the involved anatomical alterations and the possible causes of this developmental malformation. In the pectoral limb it consisted of a triplication of the alular digit, in the pelvic limb of a duplication of digit I. The live young Kestrel was observed for a period of two weeks to ascertain that it was unable to fly or procure prey on its own. After its death radiographs were taken and, apart from an eidonomic inspection including the wing claws, a detailed macroscopic dissection of the musculature of the pectoral and pelvic limbs was carried out using the ‘in-water-method’. Consecutive dissection steps were documented by a series of photographic slides. The relevant musculature, particularly that of the supernumerary digits, was recorded in proportional drawings. Subsequent to maceration of the limbs the isolated bones were reassembled according to the radiographs and also documented by means of photographs and drawings. This anatomical approach produced a reliable reconstruction of the skeletomuscular apparatus of the hyperdactylous limb parts. The eidonomic inspection revealed that at least young Kestrels may have two (alular and major digit) or even three wing claws per side. The proximal skeletal elements of both pectoral and pelvic limb were more sturdily built than in a typical Kestrel of comparable age. The proximal elements of the pelvic limb, the tarsometatarsus in particular, were shorter than in a typical Kestrel. In addition, the long axis of the tarsometatarsus was laterally bent in the transverse plane so that its proximal articular surfaces were medially inclined. Duplication of the cutaneous and osseous elements in the foot was accompanied by a duplication of some of the muscular and/or tendinous elements supplying digit I proper and the accessory digit I'. There were left-to-right asymmetries of the pedal musculature concerned. In contrast, the two accessory alular digits of each wing were almost completely devoid of musculature. Apart from atypical points of origin or insertion of the remaining distal musculture, left-to-right asymmetries and the two accessory alulae per wing, presumably, affected aerodynamic properties and resulted in flightlessness.

The dissection of the heads of three adult roe deer (Capreolus capreolus) provided evidence that this species of the Cervidae, like carnivores, lagomorphs and certain members of the Bovidae, possesses a zygomatic salivary gland. Homology of this salivary gland in ruminants and carnivores is assumed on the basis of its over-all topographic position and the number and course of its excretory ducts. The zygomatic gland of roe deer is a polystomatic gland and amounts to 0.02% of body weight. As in Saiga tatarica and Capricornis crispus (Bovidae), its secretions are predominantly serous. Its slightly alterated position in roe deer (and in bovids) seems to be caused by an evolutionary transformation of orbitotemporal proportions and the formation of a lacrimal bulla, in particular. This is an inflation of the intraorbital portion of the lacrimal bone providing ventral support to the ocular bulb. The lacrimal bulla is a late evolved character and emerges late in ontogeny. Its postnatal development in roe deer is presented. Comparison with the neonatal stage of lacrimal morphology in cattle suggests a similar ontogenetic development in the Bovidae. The adult grysbok (Raphicerus melanotis, Neotraginae, Bovidae) provides a ‘model situation’ of the primitive character state at the beginning of the evolutionary development of a lacrimal bulla. Zygomatic gland, lacrimal bulla and other structural elements of the ruminant orbitotemporal region provide an example of the interlocked evolutionary transformation of a complex system, the morphological result of which is a multi-layered compromise between several structurofunctional constraints.

Roaring in rutting Iberian red deer stags Cervus elaphus hispanicus is unusual compared to other subspecies of red deer, which radiated from the Iberian refugium after the last glacial maximum. In all red deer stags, the larynx occupies a permanent low mid-neck resting position and is momentarily retracted almost down to the rostral end of the sternum during the production of rutting calls. Simultaneous with the retraction of the larynx, male Iberian red deer pronouncedly protrude the tongue during most of their rutting roars. This poses a mechanical challenge for the vocal tract (vt) and for the hyoid apparatus, as tongue and larynx are strongly pulled in opposite directions. This study (i) examines the vocal anatomy and the acoustics of the rutting roars in free-ranging male C. e. hispanicus; (ii) establishes a potential mechanism of simultaneous tongue protrusion and larynx retraction by applying a two-dimensional model based on graphic reconstructions in single video frames of unrestrained animals; and (iii) advances a hypothesis of evaporative cooling by tongue protrusion in the males of a subspecies of red deer constrained to perform all of the exhausting rutting activities, including acoustic display, in a hot and arid season.

In goitred gazelles (Gazella subgutturosa), sexual dimorphism of larynx size and position is reminiscent of the case in humans, suggesting shared features of vocal ontogenesis in both species. This study investigates the ontogeny of nasal and oral calls in 23 (10 male and 13 female) individually identified goitred gazelles from shortly after birth up to adolescence. The fundamental frequency (f0) and formants were measured as the acoustic correlates of the developing sexual dimorphism. Settings for LPC analysis of formants were based on anatomical dissections of 5 specimens. Along ontogenesis, compared to females, male f0 was consistently lower both in oral and nasal calls and male formants were lower in oral calls, whereas the first two formants of nasal calls did not differ between sexes. In goitred gazelles, significant sex differences in f0 and formants appeared as early as the second week of life, while in humans they emerge only before puberty. This result suggests different pathways of vocal ontogenesis in the goitred gazelles and in humans.

Similar to male humans, Homo sapiens, the males of a few polygynous ruminants – red deer Cervus elaphus, fallow deer Dama dama and Mongolian gazelle Procapra gutturosa– have a more or less enlarged, low-resting larynx and are capable of additional dynamic vocal tract elongation by larynx retraction during their rutting calls. The vocal correlates of a large larynx and an elongated vocal tract, a low fundamental frequency and low vocal tract resonance frequencies, deter rival males and attract receptive females. The males of the polygynous goitred gazelle, Gazella subgutturosa, provide another, independently evolved, example of an enlarged and low-resting larynx of high mobility. Relevant aspects of the rutting behaviour of territorial wild male goitred gazelles are described. Video and audio recordings served to study the acoustic effects of the enlarged larynx and vocal tract elongation on male rutting calls. Three call types were discriminated: roars, growls and grunts. In addition, the adult male vocal anatomy during the emission of rutting calls is described and functionally discussed using a 2D-model of larynx retraction. The combined morphological, behavioural and acoustic data are discussed in relation to the hypothesis of sexual selection for male-specific deep voices, resulting in convergent features of vocal anatomy in a few polygynous ruminants and in human males.

The first scientific description of the Mongolian gazelle by Pallas (1777) already depicted a sexual dimorphism of the larynx and the thyrohyoid connection (Fig 1.1). Open image in new window

The involvement of the unique saiga nose in vocal production has been neglected so far. Rutting male saigas produce loud nasal roars. Prior to roaring, they tense and extend their noses in a highly stereotypic manner. This change of nose configuration includes dorsal folding and convex curving of the nasal vestibulum and is maintained until the roar ends. Red and fallow deer males that orally roar achieve a temporary increase of vocal tract length (vtl) by larynx retraction. Saiga males attain a similar effect by pulling their flexible nasal vestibulum rostrally, allowing for a temporary elongation of the nasal vocal tract by about 20%. Decrease of formant frequencies and formant dispersion, as acoustic effects of an increase of vtl, are assumed to convey important information on the quality of a dominant male to conspecifics, e.g. on body size and fighting ability. Nasal roaring in saiga may equally serve to deter rival males and to attract females. Anatomical constraints might have set a limit to the rostral pulling of the nasal vestibulum. It seems likely that the sexual dimorphism of the saiga nose was induced by sexual selection. Adult males of many mammalian species, after sniffing or licking female urine or genital secretions, raise their head and strongly retract their upper lip and small nasal vestibulum while inhalating orally. This flehmen behaviour is assumed to promote transport of non-volatile substances via the incisive ducts into the vomeronasal organs for pheromone detection. The flehmen aspect in saiga involves the extensive flexible walls of the greatly enlarged nasal vestibulum and is characterized by a distinctly concave configuration of the nose region, the reverse of that observed in nasal roaring. A step-by-step model for the gradual evolution of the saiga nose is presented here.

In many birds, the male reproductive tract is asymmetric with the left testis being larger than the right one. Coucals (Centropodidae) represent an exception as the asymmetry is typically reversed. Here, we describe the functional morphology of the reproductive tract of the African Black Coucal (Centropus grillii), a bird species with reversed sex-roles and a classical polyandrous mating system. In this species, the left testis has been reduced to a tiny, disk-like vestige that in almost all cases examined was not visible macroscopically. The vestigial left testis apparently does not participate in sperm production but has retained a vestigial left excurrent duct system. By contrast, the right deferent duct was engorged with sperm, suggesting a sperm storage function. Both deferent ducts opened on the tip of spectacularly long, erectile deferent duct papillae into the urodaeum of the male cloaca. Behavioural observations suggest that they may function as “pseudophalli”. Testis mass represented 0.49% of body mass, less than half the size of other classical polyandrous bird species. Assuming moderate to high levels of sperm competition this represents a paradox. Heavy demands on the energy budget while caring for altricial young may have prevented males from maintaining two testes and large bilateral sperm storage devices. Reduced testis mass may be compensated for by frequent transfer of small amounts of sperm. Female Black Coucals have not evolved any corresponding cloacal specializations, but like all other birds have sperm storage tubules.