Ilya A. Volodin

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.

Pups crying bass: vocal adaptation for avoidance of age-dependent predation risk in ground squirrels?

In most mammals, larger adult body size correlates with lower fundamental frequency and more closely spaced formants in vocalizations relative to juveniles. In alarm whistles of two free-living rodents, the speckled ground squirrel Spermophilus suslicus and yellow ground squirrel S. fulvus, these cues to body size were absent despite prominent differences in body weight and skull and larynx sizes between juveniles and adults. No significant correlations were found between the individual maximum fundamental frequency and body weight, both within age classes and for pooled samples of all animals within species. Furthermore, the mean alarm whistle maximum fundamental frequencies did not differ significantly between age classes (juvenile versus adult) in the speckled squirrel and were even significantly lower in juvenile yellow squirrels. We discuss the hypothesis that the obfuscation of vocal differences between juvenile and adult squirrels may represent a special adaptation of pup vocal behaviour—a form of “vocal mimicry,” resulting in imitation of adult vocal pattern to avoid infanticide and age-dependent predation risk.

The potential to encode sex, age, and individual identity in the alarm calls of three species of Marmotinae

In addition to encoding referential information and information about the sender’s motivation, mammalian alarm calls may encode information about other attributes of the sender, providing the potential for recognition among kin, mates, and neighbors. Here, we examined 96 speckled ground squirrels (Spermophilus suslicus), 100 yellow ground squirrels (Spermophilus fulvus) and 85 yellow-bellied marmots (Marmota flaviventris) to determine whether their alarm calls differed between species in their ability to encode information about the caller’s sex, age, and identity. Alarm calls were elicited by approaching individually identified animals in live-traps. We assume this experimental design modeled a naturally occurring predatory event, when receivers should acquire information about attributes of a caller from a single bout of alarm calls. In each species, variation that allows identification of the caller’s identity was greater than variation allowing identification of age or sex. We discuss these results in relation to each species’ biology and sociality.

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.

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.

Short-Term and Long-Term Individuality in Speckled Ground Squirrel Alarm Calls

Abstract Apart from the alerting function of alarm calls, selection may favor cues that help individuals to distinguish between reliable and unreliable callers. However, this mechanism for selective response to real and false alarms may act only if the individual characteristics of the call are stable at least for some time. Here we test this implicit assumption for the callers reliability hypothesis, studying individuality of alarm calls in a colony of free-living, individually marked speckled ground squirrels (Spermophilus suslicus). We recorded each of 20 study animals 4 times during repeated captures when calling from a live trap toward a human, with spans of 1 day, 2 weeks, and 1 year from the 1st capture. Ten alarm call notes per animal per capture were analyzed. Individual alarm call notes showed high similarity within captures but differed strongly between captures. Both multivariate analysis of variance and discriminant function analysis showed that vocal individuality decreased rapidly with an increase of the time span between recordings. However, vocal individuality always remained higher than expected random value. Examination of our data suggests that alarm calls are unstable, which contradicts the caller reliability hypothesis, because its implicit assumption of stable individual identity is not fulfilled. However, short-term stability still may be sufficient to ensure short-term individual recognition between kin and neighbors. Also, even if the alarm calls change structurally, because group members meet up daily, they can update their knowledge of the call structure of individuals, and this would likely allow them to distinguish between reliable and unreliable individuals.

The power of oral and nasal calls to discriminate individual mothers and offspring in red deer, Cervus elaphus

BackgroundIn most species, acoustical cues are crucial for mother-offspring recognition. Studies of a few species of ungulates showed that potential for individual recognition may differ between nasal and oral contact calls.ResultsVocalizations of 28 hinds and 31 calves of farmed Iberian red deer (Cervus elaphus hispanicus) were examined with discriminant function analyses (DFA) to determine whether acoustic structure of their oral and nasal contact calls encodes information about the caller’s identity. Contact calls were elicited by brief separation of individually identified animals by a distance over 10 m or by a bar fence. Both oral and nasal calls of both hinds and calves showed high potential to discriminate individuals. In hinds, individuality was significantly higher in the oral than in the nasal calls, whereas in calves, individuality was equally well expressed in both oral and nasal calls. For calves, the maximum fundamental frequency was higher and the duration was longer in oral calls than in nasal calls. For hinds, the maximum fundamental frequency and the duration were indistinguishable between oral and nasal calls. Compared to the pooled sample of oral and nasal calls, separate oral or nasal call samples provided better classifying accuracy to individual in either hinds or calves. Nevertheless, in both hinds and calves, even in the pooled sample of oral and nasal calls, the degree of individual identity was 2–3 times greater than expected by chance. For hinds that provided calls in both years, cross-validation of calls collected in 2012 with discriminant functions created with calls from 2011 showed a strong decrease of classifying accuracy to individual.ConclusionsThese results suggest different potentials of nasal and oral calls to allow the discrimination of individuals among hinds, but not among red deer calves. The high potential of individual recognition even with the pooled sample of oral and nasal calls allows mother and young to remember only one set of acoustic variables for mutual vocal recognition. Poor between-year stability of individual characteristics of hind oral and nasal calls would require updating keys to individual recognition each calving season.

Sign and strength of emotional arousal: vocal correlates of positive and negative attitudes to humans in silver foxes ( Vulpes vulpes )

Summary The hypothesis of similarity in trends of acoustic characteristics regardless of the sign of emotional arousal, positive or negative, has been advanced based on human vocalizations. For non-human mammals, testing is complicated because the same stimulus cannot evoke opposite (positive and negative) internal states, to trigger the respective vocalizations. To resolve this concern, we designed an experimental procedure using Tame and Aggressive strains of silver foxes, with genetically predetermined positive or negative emotional responses to humans respectively. We analyzed features of vocalizations produced by callers at different fox‐human distances, assuming changes in vocal responses reflect the shifts of human-related positive arousal in Tame foxes and human-related negative arousal in Aggressive foxes. Both strains showed similar trends for changes in calling rate and proportion of time spent vocalizing toward higher levels in response to greater emotional arousal, positive in Tame foxes and negative in Aggressive foxes. At the same time, strains showed distinctive trends for the proportions of different call types and maximum amplitude frequency. We infer that the variables with similar trends reflect the strength of emotional arousal, regardless of triggering internal states, whereas variables with distinctive trends are specifically related to the sign of emotion in silver fox.

Kind granddaughters of angry grandmothers: The effect of domestication on vocalization in cross-bred silver foxes

The genetic basis of the effects of domestication has previously been examined in relation to morphological, physiological and behavioural traits, but not for vocalizations. According to Belyaev [Belyaev, D.K., 1979. Destabilizing selection as a factor in domestication. J. Hered. 70, 301-308], directional selection for tame behaviour toward humans resulted in domestication. This hypothesis has been confirmed experimentally on the farm-bred silver fox Vulpes vulpes population that has undergone 45 years of artificial selection for tameness and 35 years of selection for aggressiveness. These foxes, with their precisely known attitudes toward people, provide a means of examining vocal indicators of tameness and aggressiveness to establish the genetic basis for vocal production in canids. We examined vocalizations toward people in foxes selected for tameness and aggressiveness compared to those of three kinds of crosses: Hybrids (Tame x Aggressive), A-Backcrosses (Aggressive x Hybrid) and T-Backcrosses (Tame x Hybrid). We report the effects of selection for tameness on usage and structure of different vocalizations and suggest that vocal indicators for tameness and aggressiveness toward people are discrete phenotypic traits in silver foxes.