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Savannah roars: The vocal anatomy and the impressive rutting calls of male impala (Aepyceros melampus) - highlighting the acoustic correlates of a mobile larynx.

ABSTRACT: 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.

SUBMITTER: Frey R

PROVIDER: S-EPMC7018640 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe rutting vocal display of male impala Aepyceros melampus is 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 topi Damaliscus 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.

Project description:Eurasian deer are characterized by the extraordinary diversity of their vocal repertoires. Male sexual calls range from roars with relatively low fundamental frequency (hereafter fo ) in red deer Cervus elaphus, to moans with extremely high fo in sika deer Cervus nippon, and almost infrasonic groans with exceptionally low fo 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 fo is associated with larger vocal folds, whereas high fo 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.

Project description:AbstractPrimates understand the meaning of their own and other species' alarm calls, but little is known about how they acquire such knowledge. Here, we combined direct behavioural observations with playback experiments to investigate two key processes underlying vocal development: comprehension and usage. Especifically, we studied the development of con- and heterospecific alarm call recognition in free-ranging sooty mangabeys, Cercocebus atys, across three age groups: young juveniles (1-2y), old juveniles (3-4y) and adults (> 5y). We observed that, during natural predator encounters, juveniles alarm called to a significantly wider range of species than adults, with evidence of refinement during the first four years of life. In the experiments, we exposed subjects to leopard, eagle and snake alarm calls given by other group members or sympatric Diana monkeys. We found that young juveniles' locomotor and vocal responses were least appropriate and that they engaged in more social referencing (look at adults when hearing an alarm call) than older individuals, suggesting that vocal competence is obtained via social learning. In conclusion, our results suggest that alarm call comprehension is socially learned during the juvenile stage, with comprehension preceding appropriate usage but no difference between learning their own or other species' alarm calls.Significance statementUnder natural conditions, animals do not just interact with members of their own species, but usually operate in a network of associated species. However, ontogenetic research on primate communication frequently ignores this significant element. We studied the development of con- and heterospecific alarm call recognition in wild sooty mangabeys. We found that communicative competence was acquired during the juvenile stages, with alarm call comprehension learning preceding appropriate vocal usage and with no clear difference in learning of con- and heterospecific signals. We also found that, during early stages of life, social referencing, a proactive form of social learning, was key in the acquisition of competent alarm call behaviour. Our results show that primates equally learn to interpret alarm calls from their own and other species during their early stages of life and that this learning process is refined as the animals mature.Supplementary informationThe online version contains supplementary material available at 10.1007/s00265-023-03318-6.

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Savannah roars: The vocal anatomy and the impressive rutting calls of male impala (Aepyceros melampus) - highlighting the acoustic correlates of a mobile larynx.

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