Roland Frey

How Low Can You Go? Physical Production Mechanism of Elephant Infrasonic Vocalizations

The Song of the Elephant In mammals, vocal sound production generally occurs in one of two ways, either through muscular control—as when a cat purrs or, more commonly, by air passing through the vocal folds—which occurs in humans and facilitates production of extremely high frequency bat calls. Over the past 20 years, it has been recognized that elephants can communicate through extremely low frequency infrasonic sounds. Taking advantage of a natural death of an elephant in a zoo, Herbst et al. (p. 595) examined the biomechanics of elephant sound production in an excised elephant larynx. Self-sustained vocal-fold vibrations, without the presence of any neural control, were used to produce infrasonic elephant sounds, using the same mechanism as singing in humans and echolocation in bats. Elephants produce low-frequency sounds via intrinsic vocal-fold vibrations similar to those in humans. Elephants can communicate using sounds below the range of human hearing (“infrasounds” below 20 hertz). It is commonly speculated that these vocalizations are produced in the larynx, either by neurally controlled muscle twitching (as in cat purring) or by flow-induced self-sustained vibrations of the vocal folds (as in human speech and song). We used direct high-speed video observations of an excised elephant larynx to demonstrate flow-induced self-sustained vocal fold vibration in the absence of any neural signals, thus excluding the need for any “purring” mechanism. The observed physical principles of voice production apply to a wide variety of mammals, extending across a remarkably large range of fundamental frequencies and body sizes, spanning more than five orders of magnitude.

A nose that roars: anatomical specializations and behavioural features of rutting male saiga

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.

Mobile larynx in Mongolian gazelle: Retraction of the larynx during rutting barks in male Mongolian gazelle (Procapra gutturosa Pallas, 1777).

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.

Vocal anatomy, tongue protrusion behaviour and the acoustics of rutting roars in free-ranging Iberian red deer stags (Cervus elaphus hispanicus).

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.

Developmental changes of nasal and oral calls in the goitred gazelle Gazella subgutturosa, a nonhuman mammal with a sexually dimorphic and descended larynx

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.

Nordic rattle: the hoarse vocalization and the inflatable laryngeal air sac of reindeer (Rangifer tarandus)

Laryngeal air sacs have evolved convergently in diverse mammalian lineages including insectivores, bats, rodents, pinnipeds, ungulates and primates, but their precise function has remained elusive. Among cervids, the vocal tract of reindeer has evolved an unpaired inflatable ventrorostral laryngeal air sac. This air sac is not present at birth but emerges during ontogenetic development. It protrudes from the laryngeal vestibulum via a short duct between the epiglottis and the thyroid cartilage. In the female the growth of the air sac stops at the age of 2–3 years, whereas in males it continues to grow up to the age of about 6 years, leading to a pronounced sexual dimorphism of the air sac. In adult females it is of moderate size (about 100 cm3), whereas in adult males it is large (3000–4000 cm3) and becomes asymmetric extending either to the left or to the right side of the neck. In both adult females and males the ventral air sac walls touch the integument. In the adult male the air sac is laterally covered by the mandibular portion of the sternocephalic muscle and the skin. Both sexes of reindeer have a double stylohyoid muscle and a thyroepiglottic muscle. Possibly these muscles assist in inflation of the air sac. Head‐and‐neck specimens were subjected to macroscopic anatomical dissection, computer tomographic analysis and skeletonization. In addition, isolated larynges were studied for comparison. Acoustic recordings were made during an autumn round‐up of semi‐domestic reindeer in Finland and in a small zoo herd. Male reindeer adopt a specific posture when emitting their serial hoarse rutting calls. Head and neck are kept low and the throat region is extended. In the ventral neck region, roughly corresponding to the position of the large air sac, there is a mane of longer hairs. Neck swelling and mane spreading during vocalization may act as an optical signal to other males and females. The air sac, as a side branch of the vocal tract, can be considered as an additional acoustic filter. Individual acoustic recognition may have been the primary function in the evolution of a size‐variable air sac, and this function is retained in mother–young communication. In males sexual selection seems to have favoured a considerable size increase of the air sac and a switch to call series instead of single calls. Vocalization became restricted to the rutting period serving the attraction of females. We propose two possibilities for the acoustic function of the air sac in vocalization that do not exclude each other. The first assumes a coupling between air sac and the environment, resulting in an acoustic output that is a combination of the vocal tract resonance frequencies emitted via mouth and nostrils and the resonance frequencies of the air sac transmitted via the neck skin. The second assumes a weak coupling so that resonance frequencies of the air sac are lost to surrounding tissues by dissipation. In this case the resonance frequencies of the air sac solely influence the signal that is further filtered by the remaining vocal tract. According to our results one acoustic effect of the air sac in adult reindeer might be to mask formants of the vocal tract proper. In other cervid species, however, formants of rutting calls convey essential information on the quality of the sender, related to its potential reproductive success, to conspecifics. Further studies are required to solve this inconsistency.

Sexual Dimorphism of the Larynx of the Mongolian Gazelle (Procapra gutturosa Pallas, 1777) (Mammalia, Artiodactyla, Bovidae)

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 females, 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.

Descended and mobile larynx, vocal tract elongation and rutting roars in male goitred gazelles (Gazella subgutturosa Guldenstaedt, 1780)

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 Anatomy of Vocal Divergence in North American Elk and European Red Deer

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

Spectrographic analysis points to source–filter coupling in rutting roars of Iberian red deer

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.