Bull bellows and bugles: a remarkable convergence of low and high-frequency vocalizations between male domestic cattle Bos taurus and the rutting calls of Siberian and North American wapiti

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 bugles of domestic cattle bulls provide an excellent model for comparative research with cervid bugles concerning the mechanism of vocal production and the underlying anatomical and behavioural adaptations.     

Biphonation May Function to Enhance Individual Recognition in the Dhole, Cuon alpinus

Biphonation (two independent fundamental frequencies in a call spectrum) represents one of the most widespread nonlinear phenomena in mammalian vocalizations. Recently, the structure of biphonations was described in detail; however, their functions are poorly understood. For the dhole (Cuon alpinus), biphonic calls represent a prominent feature of vocal activity. In this species, the biphonic call is composed of two frequency components – the high‐frequency squeak and the low‐frequency yap, which also occur alone as separate calls. In this study, we test the hypothesis that the complication of call structure, resulting from the joining of these calls into the biphonic yap–squeak may enhance the potential for individual recognition in the dhole. We randomly selected for analysis 30 high‐frequency squeaks, 30 low‐frequency yaps and 30 biphonic yap–squeaks per animal from five subadult captive dholes (450 calls in total). Discriminant analysis, based on 10 squeak parameter values, showed 80.7% correct assignment to a predicted individual. For 10 yap parameters, the correct assignment was only 44.7%. However, the analysis based on 10 parameters of the biphonic yap–squeak, selected as best contributing to discrimination, showed 96.7% correct assignment to a predicted individual. The results provide strong support for the hypothesis tested showing that the joining of two independent calls into a common vocalization may function to enhance individual recognition in the dhole.     

Polyphony of domestic dog whines and vocal cues to body size

In domestic dogs Canis familiaris, vocal traits have been investigated for barks and growls, and the relationship between individual body size and vocal traits investigated for growls, with less corresponding information for whines. In this study, we examined the frequency and temporal traits of whines of 20 adult companion dogs (9 males, 11 females), ranging in body mass from 3.5 to 70.0 kg and belonging to 16 breeds. Dog whines (26–71 per individual, 824 in total) were recorded in conditioned begging contexts modeled by dog owners. Whines had 3 independent fundamental frequencies: the low, the high and the ultra-high that occurred singly as monophonic calls or simultaneously as 2-voice biphonic or 3-voice polyphonic calls. From the smallest to largest dog, the upper frequency limit varied from 0.24 to 2.13 kHz for the low fundamental frequency, from 2.95 to 10.46 kHz for the high fundamental frequency and from 9.99 to 23.26 kHz for the ultra-high fundamental frequency. Within individuals, the low fundamental frequency was lower in monophonic than in biphonic whines, whereas the high fundamental frequency did not differ between those whine types. All frequency variables of the low, high, and ultra-high fundamental frequencies correlated negatively with dog body mass. For duration, no correlation with body mass was found. We discuss potential production mechanisms and sound sources for each fundamental frequency; point to the acoustic similarity between high-frequency dog whines and rodent ultrasonic calls and hypothesize that ultra-high fundamental frequencies function to allow private, “tete-a-tete” communication between members of social groups.     

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.     

Usage of monophonic and biphonic calls by free-ranging resident killer whales (Orcinus orca) in Kamchatka, Russian Far East

Killer whale discrete calls include types containing an overlapping high-frequency component (biphonic calls) and types without an overlapping high-frequency component (monophonic calls). In the resident killer whales of the Northeast Pacific, biphonic discrete calls exhibit higher source levels than monophonic calls, which suggests different active space and consequently different functions for monophonic and biphonic call types. In this study we investigate the potential communicative functions of monophonic and biphonic discrete calls produced by killer whales from Kamchatka (Northwest Pacific). We analyze how the usage of these calls depends on the number of pods present in the area and type of activity. Our results show that the usage of monophonic and biphonic calls in Kamchatkan killer whales depends on the number of pods in the area and is less dependent on the type of activity. Biphonic calls are more common when more than one pod is present in the area and could therefore function as markers of pod and matriline affiliation, serving mainly as cohesion signals. Monophonic calls dominated the vocalizations when a single pod was present, while in the presence of more than one pod both categories were used in equal proportions.     

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

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

BIPHONATION AS A PROMINENT FEATURE OF DHOLE CUON ALPINUS SOUNDS

ABSTRACT

Spectrographic analysis showed that dholes produce sounds with two fundamental frequencies (components): the high-frequency and the low-frequency, which may occur simultaneously or separately. The fundamental frequency of the low-frequency component varied from 0.52 to 1.44 kHz, and that of the high-frequency component from 5.51 to 10.77 kHz. In calls where both the frequencies occurred simultaneously, they were not integer multiples of each other. They also had different frequency modulations and had additional combinative frequency bands. These are features of biphonation. Our data showed biphonation occurs in a lot of dhole calls (20 to 92% of the calls, depending on the individual (n=14); average occurrence 44.3%, n=1317 sounds). The occurrence of biphonation did not differ between sexes and ages; however, occurrence of the high component only was significantly higher in subadult animals, whereas the occurrence of the low component only was significantly higher in adults. Based on the sound structures, we discuss probable mechanisms of sound production for both the components in the dhole. For the low component, the normal vocal folds oscillation mechanism is suggested. For the high component, four possible mechanisms of sound production are discussed. We conclude that the vortex-shedding mechanism is the most probable.     

Effects of selection for behavior, human approach mode and sex on vocalization in silver fox

This study presents a first direct comparison of vocal type, call rate and time spent vocalizing among Unselected, Tame and Aggressive strains of silver fox (Vulpes vulpes) in three modes of human approach (Provoking, Approach–Retreat, and Static). Also, it provides a first comparison of male and female vocal output in the Provoking test. Vocal types were found strain-specific irrespective of the fox sex or the test. Males had higher call rates and spent shorter times vocalizing than females. These results support the evidence of genetic-based emotional states, triggering vocal behavior in silver fox strains, and suggest sex dimorphism in vocal activity toward humans.     

A Cervid Vocal Fold Model Suggests Greater Glottal Efficiency in Calling at High Frequencies

Male Rocky Mountain elk (Cervus elaphus nelsoni) produce loud and high fundamental frequency bugles during the mating season, in contrast to the male European Red Deer (Cervus elaphus scoticus) who produces loud and low fundamental frequency roaring calls. A critical step in understanding vocal communication is to relate sound complexity to anatomy and physiology in a causal manner. Experimentation at the sound source, often difficult in vivo in mammals, is simulated here by a finite element model of the larynx and a wave propagation model of the vocal tract, both based on the morphology and biomechanics of the elk. The model can produce a wide range of fundamental frequencies. Low fundamental frequencies require low vocal fold strain, but large lung pressure and large glottal flow if sound intensity level is to exceed 70 dB at 10 m distance. A high-frequency bugle requires both large muscular effort (to strain the vocal ligament) and high lung pressure (to overcome phonation threshold pressure), but at least 10 dB more intensity level can be achieved. Glottal efficiency, the ration of radiated sound power to aerodynamic power at the glottis, is higher in elk, suggesting an advantage of high-pitched signaling. This advantage is based on two aspects; first, the lower airflow required for aerodynamic power and, second, an acoustic radiation advantage at higher frequencies. Both signal types are used by the respective males during the mating season and probably serve as honest signals. The two signal types relate differently to physical qualities of the sender. The low-frequency sound (Red Deer call) relates to overall body size via a strong relationship between acoustic parameters and the size of vocal organs and body size. The high-frequency bugle may signal muscular strength and endurance, via a ‘vocalizing at the edge’ mechanism, for which efficiency is critical.     

Diversity of the Vocal Signals of Concave-Eared Torrent Frogs (Odorrana tormota): Evidence for Individual Signatures

Male concave-eared torrent frogs ( Odorrana tormota ) have an unusually large call repertoire and have been shown to communicate ultrasonically. We investigated the individual specificity of male advertisement calls in order to explore the acoustic bases of individual recognition, which was demonstrated in an accompanying study. Vocalizations of 15 marked males were recorded in the field. A quantitative analysis of the signals revealed eight basic call-types. Two of them (the single- and multi-note long-calls) were investigated in more detail. Long-calls were characterized by pronounced and varying frequency modulation patterns, and abundant occurrence of nonlinear phenomena (NLP), i.e., frequency jumps, subharmonics, biphonations and deterministic chaos. The occurrence of NLP was predictable from the contour of the fundamental frequency in the harmonic segment preceding the onset of the NLP, and this prediction showed individual-specific patterns. Fifteen acoustic variables of the long calls were measured, all of which were significantly different among individuals, except biphonic segment duration. Discriminant function analysis (DFA) showed that 54.6% of the calls could be correctly assigned to individual frogs. The correct classification was above chance level, suggesting that individual specificity of calls underlie the ability of males to behaviorally discriminate the vocal signals of their neighbors from those of strangers, a remarkable feat for a frog species with a diverse vocal repertoire. The DFA classification results were lower than those for other anurans, however. We hypothesize that there is a tradeoff between an increase in the fundamental frequency of vocalizations to avoid masking by low-frequency ambient background noise, and a decrease in individual-specific vocal tract information extractable from the signal.     

Oestrous red deer hinds prefer male roars with higher fundamental frequencies

Across vertebrates, the observation that lower-pitched vocalizations are typically associated with larger and/or higher quality males has lead to the widespread belief that inter- and intra-sexual selection will produce male calls with low fundamental frequencies (F0). Here we investigated the response of oestrous red deer hinds to playback of re-synthesized male roars characterized by either higher than average or lower than average F0. We found that hinds prefer higher rather than lower ‘pitched’ roars, providing, to our knowledge, the first evidence of such a bias in nonhuman mammals. Our findings can be interpreted in relation to previous observations that the minimum F0 of roars is positively correlated with male reproductive success in free-ranging red deer stags, and that across Cervids the F0 of male mating calls shows extreme variability. Females showing preferences for higher-pitched roars might derive genetic benefits through more competitive male offspring. Our results emphasize the need for further investigations of female preferences in mammals in order to better understand the extreme variation of F0 values observed in male sexual calls.     

Variability of CAG tandem repeats in exon 1 of the androgen receptor gene is not related with dog intersexuality

Numerous mutations of the human androgen receptor (AR) gene cause an intersexual phenotype, called the androgen insensitivity syndrome. The intersexual phenotype is also quite often diagnosed in dogs. The aim of this study was to conduct a comparative analysis of the entire coding sequence (eight exons) of the AR gene in healthy and four intersex dogs, as well as in three other canids (the red fox, arctic fox and Chinese raccoon dog). The coding sequence of the studied species appeared to be conserved (similarity above 97%) and polymorphism was found in exon 1 only. Altogether, 2 SNPs were identified in healthy dogs, 14 in red foxes, 16 in arctic foxes and 6 were found in Chinese raccoon dogs, respectively. Moreover, a variable number of tandem repeats (CAG and CAA), encoding an array of glutamines, was also observed in this exon. The CAA codon numbers were invariable within species, but the CAG repeats were polymorphic. The highest number of the CAG and CAA repeats was found in dogs (from 40 to 42) and the observed variability was similar in intersex and healthy dogs. In the other canids the variability fell within the following ranges: 29–37 (red fox), 37–39 (arctic fox) and 29–32 (Chinese raccoon dog). In addition, a polymorphic microsatellite marker in intron 2 was found in the dog, red fox and Chinese raccoon dog. It was concluded that the polymorphism level of the AR gene in the dog was lower than in the other canids and none of the detected polymorphisms, including variability of the CAG tandem repeats, could be related with the intersexual phenotype of the studied dogs.     

The Acoustic Structure and Information Content of Female Koala Vocal Signals

Determining the information content of animal vocalisations can give valuable insights into the potential functions of vocal signals. The source-filter theory of vocal production allows researchers to examine the information content of mammal vocalisations by linking variation in acoustic features with variation in relevant physical characteristics of the caller. Here I used a source-filter theory approach to classify female koala vocalisations into different call-types, and determine which acoustic features have the potential to convey important information about the caller to other conspecifics. A two-step cluster analysis classified female calls into bellows, snarls and tonal rejection calls. Additional results revealed that female koala vocalisations differed in their potential to provide information about a given caller’s phenotype that may be of importance to receivers. Female snarls did not contain reliable acoustic cues to the caller’s identity and age. In contrast, female bellows and tonal rejection calls were individually distinctive, and the tonal rejection calls of older female koalas had consistently lower mean, minimum and maximum fundamental frequency. In addition, female bellows were significantly shorter in duration and had higher fundamental frequency, formant frequencies, and formant frequency spacing than male bellows. These results indicate that female koala vocalisations have the potential to signal the caller’s identity, age and sex. I go on to discuss the anatomical basis for these findings, and consider the possible functional relevance of signalling this type of information in the koala’s natural habitat.     

Variability of Female Responses to Conspecific vs. Heterospecific Male Mating Calls in Polygynous Deer: An Open Door to Hybridization?

Males of all polygynous deer species (Cervinae) give conspicuous calls during the reproductive season. The extreme interspecific diversity that characterizes these vocalizations suggests that they play a strong role in species discrimination. However, interbreeding between several species of Cervinae indicates permeable interspecific reproductive barriers. This study examines the contribution of vocal behavior to female species discrimination and mating preferences in two closely related polygynous deer species known to hybridize in the wild after introductions. Specifically, we investigate the reaction of estrous female red deer (Cervus elaphus) to playbacks of red deer vs. sika deer (Cervus nippon) male mating calls, with the prediction that females will prefer conspecific calls. While on average female red deer preferred male red deer roars, two out of twenty females spent more time in close proximity to the speaker broadcasting male sika deer moans. We suggest that this absence of strict vocal preference for species-specific mating calls may contribute to the permeability of pre-zygotic reproductive barriers observed between these species. Our results also highlight the importance of examining inter-individual variation when studying the role of female preferences in species discrimination and intraspecific mate selection.     

Interspecific killing between wolves and golden jackals in Iran

Interspecific killing is a widespread phenomenon among mammalian carnivores; being common, for instance, within the canid guild. The canid guild in Hamadan province, west of Iran, comprises three species: the gray wolf Canis lupus pallipes, the golden jackal Canis aureus, and the red fox Vulpes vulpes. In this area, habitat transformation and agricultural land uses have significantly reduced wild prey populations. In search of food, members of the canid guild are often driven to human settlements. Due to inefficient waste management, the major source of food for canids here is anthropogenic food resources, such as livestock and pet carcasses, and domestic waste illegally dumped near poultry farms and rural areas. Here, we described one of the first reports in the literature of a case of interspecific killing between a wolf and a golden jackal. On June 13, 2016, a collared wolf (adult male) killed an adult jackal (adult male). Further studies are required to understand intraguild competition among red fox, golden jackals, and wolves in this area.     

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 × Aggressive), A-Backcrosses (Aggressive × Hybrid) and T-Backcrosses (Tame × 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.     

Bat echolocation calls facilitate social communication

Bat echolocation is primarily used for orientation and foraging but also holds great potential for social communication. The communicative function of echolocation calls is still largely unstudied, especially in the wild. Eavesdropping on vocal signatures encoding social information in echolocation calls has not, to our knowledge, been studied in free-living bats so far. We analysed echolocation calls of the polygynous bat Saccopteryx bilineata and found pronounced vocal signatures encoding sex and individual identity. We showed experimentally that free-living males discriminate approaching male and female conspecifics solely based on their echolocation calls. Males always produced aggressive vocalizations when hearing male echolocation calls and courtship vocalizations when hearing female echolocation calls; hence, they responded with complex social vocalizations in the appropriate social context. Our study demonstrates that social information encoded in bat echolocation calls plays a crucial and hitherto underestimated role for eavesdropping conspecifics and thus facilitates social communication in a highly mobile nocturnal mammal.     

Female Sexual Preferences Toward Conspecific and Hybrid Male Mating Calls in Two Species of Polygynous Deer, <Emphasis Type="Italic">Cervus elaphu</Emphasis>s and <Emphasis Type="Italic">C. nippon</Emphasis>

The behavioral processes at the basis of hybridization and introgression are understudied in terrestrial mammals. We use a unique model to test the role of sexual signals as a reproductive barrier to introgression by investigating behavioral responses to male sexual calls in estrous females of two naturally allopatric but reproductively compatible deer species, red deer and sika deer. Previous studies demonstrated asymmetries in acoustic species discrimination between these species: most but not all female red deer prefer conspecific over sika deer male calls while female sika deer exhibit no preference differences. Here, we extend this examination of acoustic species discrimination to the role of male sexual calls in introgression between parent species and hybrids. Using two-speaker playback experiments, we compared the preference responses of estrous female red and sika deer to male sexual calls from conspecifics versus red × sika hybrids. These playbacks simulate early secondary contact between previously allopatric species after hybridization has occurred. Based on previous conspecific versus heterospecific playbacks, we predicted that most female red deer would prefer conspecific calls while female sika deer would show no difference in their preference behaviors toward conspecific and hybrid calls. However, results show that previous asymmetries did not persist as neither species exhibited more preferences for conspecific over hybrid calls. Thus, vocal behavior is not likely to deter introgression between these species during the early stages of sympatry. On a wider scale, weak discrimination against hybrid sexual signals could substantially contribute to this important evolutionary process in mammals and other taxa.     

Effects of free-ranging,semi-captive and captive management on the acoustics of male rutting calls in Siberian wapiti <Emphasis Type="Italic">Cervus elaphus sibiricus</Emphasis>

In male European red deer Cervus elaphus, rutting calls that are responsible for male reproductive success are higher in fundamental frequency in captivity than in the wild. This study compares the acoustics of stag rutting calls among wild-living, semi-captive and captive stags within an Asian subspecies of C. elaphus, the Siberian wapiti Cervus elaphus sibiricus. Male Siberian wapiti rutting calls (bugles) were collected using automated recording systems in three populations (wild-living, semi-captive and captive), all originated from the Altai/Khakasian region of Central Siberia (Russia). Selected 435 bugles (145 per population) were analysed spectrographically for 14 variables of the bugle high (>1 kHz) fundamental frequency (g0) and scored for shape of g0 contour: trapeze, descending or saddle. Among bugles, 74.3% had the trapeze contour, 23.7% had the descending contour and 2.1% had the saddle contour. The additional low (<0.2 kHz) fundamental frequency (f0) was found in 76.1% of bugles, whereas deterministic chaos was found in 16.8% of bugles. Bugles of captive stags were shortest and highest in frequency. The captive management selectively affected only bugles with the trapeze contour, whereas bugles with descending contour remained unaffected by variations of deer holding regime. Stag rutting bugles are subspecies-specific and may therefore serve as acoustic indicator of subspecies for the Siberian wapiti among other Asian and American subspecies of wapiti.