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Phenotype constrains the vocal tract in the most dimorphic mammal, the southern elephant seal
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The study of mammal acoustic communication was revolutionized by the application of the source-filter theory, originally developed for human speech. The theory states that the vocal tract is constrained by body anatomy and, therefore, creates a structural link between phenotype and acoustic formants, providing a basis for honest signalling. The phenotype-formants link was validated in many species, but the phenotype-vocal tract link was rarely assessed. We used 2D videogrammetry to estimate the vocal tract length of wild southern elephant seal males (Mirounga leonina Linnaeus, 1758) during their normal vocalization behaviour. We showed that: 1) the vocal tract can be measured non-invasively in a wild large mammal; 2) the vocal tract depends on the structural phenotype (age, body length, and skull size); 3) the nasal tract is more related to the structural phenotype than the buccal tract; 4) the dependence on size, and body length in particular, is stronger than the dependence on age. All together, the phenotypic constraint on vocal tract provides the anatomical basis for honest signalling in elephant seals.
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Acoustic allometry is the study of how animal vocalizations reflect their body size. A key aim of this research is to identify outliers to acoustic allometry principles and pinpoint the evolutionary origins of such outliers. A parallel strand of research investigates species capable of vocal learning, the experience-driven ability to produce novel vocal signals through imitation or modification of existing vocalizations. Modification of vocalizations is a common feature found when studying both acoustic allometry and vocal learning. Yet, these two fields have only been investigated separately to date. Here, we review and connect acoustic allometry and vocal learning across mammalian clades, combining perspectives from bioacoustics, anatomy and evolutionary biology. Based on this, we hypothesize that, as a precursor to vocal learning, some species might have evolved the capacity for volitional vocal modulation via sexual selection for ‘dishonest’ signalling. We provide preliminary support for our hypothesis by showing significant associations between allometric deviation and vocal learning in a dataset of 164 mammals. Our work offers a testable framework for future empirical research linking allometric principles with the evolution of vocal learning.
Research in ecology and wildlife biology remains crucial for increasing our knowledge and improving species management and conservation in the midst of the current biodiversity crisis. However, obtaining information on population status often involves invasive sampling of a certain number of individual animals. Marking and sampling practices include taking blood and tissue samples, toe-clipping of amphibians and rodents, or using implants and radio-transmitters – techniques that can negatively affect the animal. Wildlife research may then result in a fundamental conflict between individual animal welfare and the welfare of the population or ecosystem, which could be significantly reduced if non-invasive research practices were more broadly implemented. Implementation of non-invasive methods could be guided by the so-called 3Rs principles for animal research (replace, reduce, refine), which were proposed by Russell and Burch 60 years ago and have become a part of many animal protection legislations worldwide. However, the process of incorporating the 3Rs principles into wildlife research has been unfortunately rather slow and their importance overlooked. In order to help alleviate this situation, here I provide an overview of the most common practices in wildlife research, discuss their potential impact on animal welfare, and present available non-invasive alternatives.
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.
The elephant seal (genus Mirounga) proboscis is a textbook example of an exaggerated secondary sexual trait, whose function is debated. The proboscis can be related to sexual status advertising, emission of aggressive vocalizations, and/or female mating choice. The study of the proboscis is complicated, because it is a soft trait that needs to be studied when males vocalize and it is thus expanded. Here, we combined field stimulation experiments, 2D photogrammetry, and geometric morphometrics, to study the proboscis of wild elephant seals in natural conditions. The goal of our study was twofold: (a) to demonstrate that photogrammetry and geometric morphometrics can be effectively applied in the field to wild, large, non-sedated mammals; (b) to study the proboscis shape development during maturation. We found that it is possible to accurately estimate the proboscis size and shape using photographs of vocalizing males taken in the field. Moreover, we showed that mature and non-mature males differ not only in proboscis size but also in its shape, a difference that is largely allometric and can have important effects on the frequency structure and individual signature of male vocalizations. These results open new avenues for future research on this enigmatic structure, its function in aggressive displays and potential role in sexual selection, and also exemplify a very promising approach, that could be applied in field studies of other large mammals.
Vocal dialects are fundamental to our understanding of the transmission of social behaviours between individuals and populations, however few accounts trace this phenomenon among mammals over time. Northern elephant seals (Mirounga angustirostris) provide a rare opportunity to examine the trajectory of dialects in a long-lived mammalian species. Dialects were first documented in the temporal patterns of the stereotyped vocal displays produced by breeding males at four sites in the North Pacific in 1968 and 1969, as the population recovered from extreme exploitation. We evaluated the longevity of these geographical differences by comparing these early recordings to calls recently recorded at these same locations. While the presence of vocal dialects in the original recordings was re-confirmed, geographical differences in vocal behaviour were not found at these breeding rookeries nearly 50 years later. Moreover, the calls of contemporary males displayed more structural complexity after approximately four generations, with substantial between-individual variation and call features not present in the historical data. In the absence of measurable genetic variation in this species-owing to an extreme population bottleneck-a combination of migration patterns and cultural mutation are proposed as factors influencing the fall of dialects and the dramatic increase in call diversity.
A fundamental issue in the evolution of communication is the degree to which signals convey accurate (" honest ") information about the signaler. In bioacoustics, the assumption that fundamental frequency (fo) should correlate with the body size of the caller is widespread, but this belief has been challenged by various studies, possibly because larynx size and body size can vary independently. In the present comparative study, we conducted excised larynx experiments to investigate this hypothesis rigorously and explore the determinants of f o. Using specimens from eleven primate species, we carried out an inter-specific investigation, examining correlations between the minimum fo produced by the sound source, body size and vocal fold length (VFL). We found that, across species, VFL predicted minimum f o much better than body size, clearly demonstrating the potential for decoupling between larynx size and body size in primates. These findings shed new light on the diversity of primate vocalizations and vocal morphology, highlighting the importance of vocal physiology in understanding the evolution of mammal vocal communication.
A fundamental assumption in bioacoustics is that large animals tend to produce vocalizations with lower frequencies than small animals. This inverse relationship between body size and vocalization frequencies is widely considered to be foundational in animal communication, with prominent theories arguing that it played a critical role in the evolution of vocal communication, in both production and perception. A major shortcoming of these theories is that they lack a solid empirical foundation: rigorous comparisons between body size and vocalization frequencies remain scarce, particularly among mammals. We address this issue here in a study of body size and vocalization frequencies conducted across 91 mammalian species, covering most of the size range in the orders Primates (n = 50; ~0.11–120 Kg) and Carnivora (n = 41; ~0.14–250 Kg). We employed a novel procedure designed to capture spectral variability and standardize frequency measurement of vocalization data across species. The results unequivocally demonstrate strong inverse relationships between body size and vocalization frequencies in primates and carnivores, filling a long-standing gap in mammalian bioacoustics and providing an empirical foundation for theories on the adaptive function of call frequency in animal communication.
For four decades, the inability of nonhuman primates to produce human speech sounds has been claimed to stem from limitations in their vocal tract anatomy, a conclusion based on plaster casts made from the vocal tract of a monkey cadaver. We used x-ray videos to quantify vocal tract dynamics in living macaques during vocalization, facial displays, and feeding. We demonstrate that the macaque vocal tract could easily produce an adequate range of speech sounds to support spoken language, showing that previous techniques based on postmortem samples drastically underestimated primate vocal capabilities. Our findings imply that the evolution of human speech capabilities required neural changes rather than modifications of vocal anatomy. Macaques have a speech-ready vocal tract but lack a speech-ready brain to control it.
Recent studies have revealed that some mammals possess adaptations that enable them to produce vocal signals with much lower fundamental frequency (F0) and formant frequency spacing (DF) than expected for their size. Although these adaptations are assumed to reflect selection pressures for males to lower frequency components and exaggerate body size in reproductive contexts, this hypothesis has not been tested across a broad range of species. Here we show that male terrestrial mammals produce vocal signals with lower DF (but not F0) than expected for their size in mating systems with greater sexual size dimorphism. We also reveal that males produce calls with higher than expected F0 and DF in species with increased sperm competition. This investigation confirms that sexual selection favours the use of DF as an acoustic size exaggerator and supports the notion of an evolutionary trade-off between pre-copulatory signalling displays and sperm production.
Research on the evolution of human speech and music benefits from hypotheses and data generated in a number of disciplines. The purpose of this article is to illustrate the high relevance of pinniped research for the study of speech, musical rhythm, and their origins, bridging and complementing current research on primates and birds. We briefly discuss speech, vocal learning, and rhythm from an evolutionary and comparative perspective. We review the current state of the art on pinniped communication and behavior relevant to the evolution of human speech and music, showing interesting parallels to hypotheses on rhythmic behavior in early hominids. We suggest future research directions in terms of species to test and empirical data needed.
The information conveyed in acoustic signals is a central topic in mammal vocal communication research. Body size is one form of information that can be encoded in calls. Acoustic allometry aims to identify the specific acoustic correlates of body size within the vocalizations of a given species, and formants are often a useful acoustic cue in this context. We conducted a longitudinal investigation of acoustic allometry in domestic piglets (Sus scrofa domesticus), asking whether formants of grunt vocalizations provide information concerning the caller's body size over time. On four occasions, we recorded grunts from 20 Kune Kune piglets, measured their vocal tract length by means of radiographs (X-rays) and weighed them. Controlling for effects of age and sex, we found that body weight strongly predicts vocal tract length, which in turn determines formant frequencies. We conclude that grunt formant frequencies could allow domestic pigs to assess a signaler's body size as it grows. Further research using playback experiments is needed to determine the perceptual role of formants in domestic pig communication.
Males often face a trade-off between investments in precopulatory and postcopulatory traits [1], particularly when male-male contest competition determines access to mates [2]. To date, studies of precopulatory strategies have largely focused on visual ornaments (e.g., coloration) or weapon morphology (e.g., antlers, horns, and canines). However, vocalizations can also play an important role in both male competition and female choice [3–5]. We investigated variation in vocal tract dimensions among male howler monkeys (Alouatta spp.), which produce loud roars using a highly specialized and greatly enlarged hyoid bone and larynx [6]. We examined the relative male investment in hyoids and testes among howler monkey species in relation to the level of male-male competition and analyzed the acoustic consequences of variation in hyoid morphology. Species characterized by single-male groups have large hyoids and small testes, suggesting high levels of vocally mediated competition. Larger hyoids lower formant frequencies, probably increasing the acoustic impression of male body size and playing a role analogous to investment in large body size or weaponry. Across species, as the number of males per group increases, testes volume also increases, indicating higher levels of postcopulatory sperm competition, while hyoid volume decreases. These results provide the first evidence of an evolutionary trade-off between investment in precopulatory vocal characteristics and postcopulatory sperm production.
It is not always practical to hand-measure body size of free-ranging animals. In recent years, parallel-laser photogrammetry has become increasingly common for obtaining remote estimates of body size. However, it is unknown how well this technique might capture variation in body size of curvilinear features or whether the distance between parallel-laser calipers is altered when projected onto a curved surface. We describe a photogrammetric system that may be useful for obtaining body-size measurements from unrestrained large mammals that permit approach. We tested the use of parallel-laser photogrammetry to estimate the size of curvilinear features in domestic horses (Equus ferus caballus) and identified morphometrics that explained variation in body weight. Despite projecting the lasers onto a curved surface (the barrel of a horse), we achieved accurate photogrammetric estimates of linear hand-measurements. The curvilinear hand-measurements also showed strong correlations (R2 ≥ 0.996) with their respective linear photogrammetric estimates, and most photogrammetric estimates had high reliability. Using 3 variables of body size, photogrammetric estimates and hand-measurements explained 86.0% and 96.2% of the variation in weight, respectively. © 2015 The Wildlife Society.
The southern elephant seal (Mirounga leonina (L., 1758)) is one of the most dimorphic mammals, but sexual dimorphism in its skull ontogeny is poorly known. We study ontogeny of sexual dimorphism by the allometric relationships between 21 measurements and its geometric mean. Based on 66 specimens (36 females, 30 males), the bivariate and multivariate analyses indicated that both approaches were congruent in most variables. We detected that sexual dimorphism was reached mostly by sexual shape differences in the ontogenetic trajectories of males and females. Twenty-four percent of variables were associated with intercept differences (pup size proportions), while 57% of variables were associated with slope intersexual differences (relative growth rates). Contrarily, sexual dimorphism was also achieved by size differences in adult stages (19% of variables), as males exhibited an extension of their common ontogenetic trajectories. Secondary growth spurt in males was detected for few variables. Our comparison with analogous data collected from southern sea lions (Otaria byronia (de Blainville, 1820)) indicated that in both species, sexual dimorphism was mostly associated with an enhanced ability to defend territories, which was linked to the polygynic behavior. However, discrepancies between both ontogenetic patterns of dimorphism were associated with interspecific differences in their life cycles.
Body size is an important determinant of resource and mate competition in many species. Competition is often mediated by conspicuous vocal displays, which may help to intimidate rivals and attract mates by providing honest cues to signaler size. Fitch proposed that vocal tract resonances (or formants) should provide particularly good, or honest, acoustic cues to signaler size because they are determined by the length of the vocal tract, which in turn, is hypothesized to scale reliably with overall body size. There is some empirical support for this hypothesis, but to date, many of the effects have been either mixed for males compared with females, weaker than expected in one or the other sex, or complicated by sampling issues. In this paper, we undertake a direct test of Fitch's hypothesis in two canid species using large samples that control for age- and sex-related variation. The samples involved radiographic images of 120 Portuguese water dogs Canis lupus familiaris and 121 Russian silver foxes Vulpes vulpes. Direct measurements were made of vocal tract length from X-ray images and compared against independent measures of body size. In adults of both species, and within both sexes, overall vocal tract length was strongly and significantly correlated with body size. Effects were strongest for the oral component of the vocal tract. By contrast, the length of the pharyngeal component was not as consistently related to body size. These outcomes are some of the clearest evidence to date in support of Fitch's hypothesis. At the same time, they highlight the potential for elements of both honest and deceptive body signaling to occur simultaneously via differential acoustic cues provided by the oral versus pharyngeal components of the vocal tract.
Male vocalisations have an important role in mating tactics, breeding strategies and sexual selection. Most studies of vocalisations are concentrated on the time and frequency domains, while the intensity of sound, an important acoustic parameter that should be related to body size, is almost completely ignored as a possible honest signal of resource holding potential (RHP) and cue for mate choice. In this paper, we analyse the repeatability, the correlations with age and size, and the relationship with breeding status of source level (SL) of male vocalisations in the two species of elephant seals (Mirounga leonina and M. angustirostris). We found a high repeatability of SL, equal or higher than the repeatability of frequency domain parameters estimated in a previous study. Southern elephant seal males were significantly larger and produce significantly more powerful vocalisations than northern males. Moreover, in each species SL was related to age, body size, and breeding status of males, but relationships were weak and accounted for just a small proportion of SL variance. We conclude that, although SL may be an honest signal of gross differences of RHP, it is not, by itself, a good candidate for the transmission of high-resolution information on individual phenotype. A combination of SL and frequency components could be, on the contrary, an effective way to communicate RHP.
Southern elephant seal Mirounga leonina males have a complex and stereotyped system of access to breeding females. The single most important component of male behaviour is vocal signalling, which is used to settle agonistic encounters in most cases. Most aspects of the breeding biology of the species have been studied in depth, but detailed information about the structure of vocalisations is not readily available. Here, we present data about the acoustic structure of aggressive male vocalisations collected in the Falkland Islands and we compare these data to published data on the northern elephant seals. Our main goal is to describe the structure of sounds as a preliminary and indispensable step towards analysis of their functional significance.Male vocalisations are low-pitched sounds, made up of pulse trains, with little frequency modulation. Low frequency and high sound pressure level are typical of male vocalisations in Pinnipedia, but they were particularly evident in southern elephant seals, probably due to the unusually large body size. The comparison with published data on northern elephant seals was not very easy, due to differences in acoustic terminology and methodology, but it revealed many similarities between the species.We also carried out a detailed analysis of variability of different acoustic variables. We discovered that frequency and intensity measures have lower variability than temporal ones and should hence be the most effective way to convey information about the individual who emits the vocalisation.
Inequality in distribution of resources is a key aspect of evolutionary biology particularly in relation to distribution of mates and copulations. Notwithstanding its important role, inequality is not easily defined, and its measurement is complicated by theoretical and methodological issues. Although the formal treatment of inequality has been mostly limited to the evolution of lek mating system, a methodologically correct approach to measurement of inequality is generally valid for the study of any kind of mating system. In this paper, we analyze inequality in a large set of southern elephant seal (Mirounga leonina) harems. The observed distribution of fertilizations was significantly different from both the expected distribution with equal shares of resources and the expected distribution with equal propensities to acquire resources. We calculate and compare various measures of inequality, observing a wide variation particularly among unbounded and bounded indices. We check the effect of choosing a specific measure of inequality by considering the effect of two aspects of harem socionomy, the number of females in the harem (i.e., the total amount of resources to be shared) and the number of males associated with the harem (i.e., the number of competitors). The choice of a specific measure of inequality had a strong impact on the results obtained and should be considered a critical step in every study of functional and evolutionary correlates of inequality. Unbounded indices showed a strong relationship with both harem size and number of males, while no effect was evident in the analysis of bounded indices. This demonstrates that, in this species, the despotism of the mating system remains high even in large harems and with many competitors, i.e., the worst conditions for monopolization.
In traditional studies of animal communication, individual variability was sometimes considered less relevant than species specific aspects, mostly because the goal was the classifications of sounds in repertories. However, individual variability seems to have a significant role in signal function and evolution. In this paper, we analyse individual variation in the structure of aggressive vocalisations of male southern elephant seals and we compare sounds from our main study population, Sea Lion Island (Falkland Islands), with sounds recorded in the nearby population of the Valdés Peninsula (Patagonia, Argentina).We firstly analysed the repeatability of acoustic parameters at vocalisation and male level. Repeatability of bouts of the same vocalisation was extremely high and this confirmed that vocalisation is the fundamental level of organisation of male acoustic communication in this species. Also repeatability of vocalisations of individual males was very high and hence sounds may effectively convey information about identity of the individual who emits the sound.Male aggressive vocalisations were categorised into a small number of types and each male emitted always the same type of vocalisation. We compared the typology of sounds emitted by Sea Lion Island males with vocalisations by Valdés Peninsula males and we found striking differences. The two populations shared none of the sound types and, although similar in fundamental acoustics, sounds from the two populations had a different macrostructure. We conclude that these two populations show dialects in male acoustic communication, although the scarcity of recordings from other populations limits the scope of this conclusion.
Introduction
The nature of the following work will be best understood by a brief account of how it came to be written. During many years I collected notes on the origin or descent of man, without any intention of publishing on the subject, but...
Dominance hierarchies structure the adult social networks of many mammals. To identify the conditions that support the establishment of stable hierarchical relationships within groups of familiar rivals, we explored the ontogeny of spatial, social and communicative behaviour among male northern elephant seals, Mirounga angustirostris. We demonstrate that as male seals reach sexual maturity, they increase residency time ashore and restrict fine-scale movement patterns within the breeding colony. This spatiotemporal overlap creates a predictable social environment in which repeated interactions promote greater social connectivity between older individuals. Moreover, as males become physically and behaviourally mature, their ritualized vocal displays transition from highly variable calls to stable and unique individual acoustic signatures, supporting recognition between familiar competitors. The developmental onset of reliable signature calls – along with concurrent changes in space occupancy – coincide with the formation of stable, structured dominance relationships among top-level competitors. These findings advance our understanding of the ontogeny of social behaviour under conditions of extreme competition.
The process of learning plays a pivotal role when an animal must correctly identify individuals within a dynamic social group. In male–male competition for access to reproductive success, a male’s ability to learn the calls that are associated with one’s rival can help to maintain structured dominance relationships and reduce the costs associated with fighting. Male northern elephant seals operate in one of the most competitive breeding systems among mammals, and selection pressures for accurate rival assessment are extreme. Through a long-term field effort that has tracked individual males over multiple breeding seasons, we have found that male elephant seals are operating in a large, spatially dynamic social network, which is conducive to the emergence of individual acoustic recognition and associative learning. Given their accessibility during the breeding season, the northern elephant seal provides an excellent comparative framework for studies of the relationship between signal function and an individual’s social environment.
Northern elephant seals (Mirounga angustirostris) are massive, land-breeding marine mammals that produce loud, stereotyped calls during annual breeding seasons. To determine vocalization source levels emitted by competing males on a mainland breeding rookery, aerial calls were measured on-axis at 1 m from adult males using three different sound pressure level metrics. Time-averaged (1 min) ambient noise was also measured under variable environmental and social conditions. Results indicate that male northern elephant seals emit high amplitude airborne calls with little variation in call amplitude. Mean source levels ranged from 98 to 114 dB re: 20 μPa [root-mean-square (rms) -fast], 102–116 dB re: 20 μPa (rms-impulse), and 120–131 dB re: 20 μPa (peak) and average standard deviations for all metrics were <2.3 dB. Further, these seal rookeries exhibit high variability in ambient noise (in terms of both spectrum and amplitude) from biotic and environmental sources. Finally, males sampled did not adjust call amplitude to compensate for higher background noise levels and thus did not exhibit a Lombard effect. These findings reinforce the view that the remarkable vocalizations of male northern elephant seals serve as rigid and powerful signals that convey individual identity within noisy breeding colonies rather than as honest indicators of size, status, or motivation.
Life‐history trade‐off theory predicts that current reproduction can negatively affect survival and future reproduction. Few studies have assessed breeding costs for males of polygynous species compared to females, despite substantial variation in breeding success among individual males (e.g. subordinate cf. dominant breeders). Specifically, differentiating between the cost of attending breeding events, and the additional cost of successfully securing and mating females is lacking.
We investigated whether trade‐offs are present in the highly polygynous male southern elephant seal Mirounga leonina using 34 years of individual‐level data. We compare age‐specific survival, recruitment and future breeding success probabilities of pre‐breeders (males yet to recruit) and breeders (subordinate and dominant social ranks) using multievent models.
Pre‐breeders and breeders of overlapping ages had similar survival probabilities, suggesting that there was no attendance cost for early recruits. In addition, the probability of recruiting as a dominant breeder never exceeded recruitment probability as a subordinate breeder of the same age. Therefore, older pre‐breeders that delayed attendance costs generally did not improve their breeding success (probability of being dominant) at recruitment more than younger recruits. Rather, recruitment age may be a function of individual quality, with lower quality individuals requiring more time to socially mature.
When comparing subordinate and dominant breeders, we found clear evidence for survival senescence, with subordinate breeders having a higher baseline mortality. In contrast, age‐specific future breeding success (probability of being dominant at t + 1) increased with age, with dominant breeders maintaining higher subsequent breeding success than subordinate breeders.
The opposite trends in survival and future breeding success for both subordinate and dominant breeders may indicate a lifetime, population‐level trade‐off. However, we found no evidence to suggest that being a dominant breeder consecutively (and having a higher accumulated breeding cost) accelerated the rate of senescence when compared to individuals that were previously subordinate.
Thus, males experienced actuarial senescence regardless of social rank, with dominant (and possibly high quality) breeders showing a reduced trade‐off between survival and future breeding success. We make several novel contributions to understanding polygynous male life histories and southern elephant seal demography.
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 adult male fallow deer specimens with artificially extended vocal tracts and measured the cross-sectional areas of the supra-laryngeal vocal tract along the oral and nasal tracts. The CT data was then used to predict the resonances produced by three possible configurations, including the oral vocal tract only, the nasal vocal tract only, or combining both. 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 nonhuman mammal vocalisation, and suggests that the potential for nasalization in putative oral loud-calls should be carefully considered.
The evolutionary origin of rhythm perception, a cognitive ability essential to musicality, remains unresolved [1-5]. The ability to perceive and memorize rhythmic sounds is widely shared among humans [6] but seems rare among other mammals [7, 8]. Although the perception of temporal metrical patterns has been found in a few species, this ability has only been demonstrated through behavioral training [9] (but see [10] for an example of spontaneous tempo coordination in a bonobo), and there is no experimental evidence to indicate its biological function. Furthermore, there is no example of a non-human mammal able to remember and recognize auditory rhythmic patterns among a wide range of tempi. In the northern elephant seal Mirounga angustirostris, the calls of mature males comprise a rhythmic series of pulses, with the call of each individual characterized by its tempo and timbre; these individual vocal signatures are stable over years and across contexts [11]. Here, we report that northern elephant seal males routinely memorize and recognize the unique tempo and timbre of their rivals' voices and use this rhythmic information to individually identify competitors, which facilitates navigation within the social network of the rookery. By performing playbacks with natural and modified vocalizations, we show that males are sensitive to call rhythm disruption independently of modification of spectral features and that they use both temporal and spectral cues to identify familiar rivals. While spectral features of calls typically encode individual identity in mammalian vocalizations [12], this is the first example of this phenomenon involving sound rhythm.
Over 40 years ago, Peter Marler proposed that animal signals were adaptive because they provided listeners with information (Marler, 1961, Journal of Theoretical Biology, 1, 295–317). But what was the nature of this information? How did it influence behaviour? And how might the information in animal signals compare with the information in human language? Here we review evidence that signals in a variety of social contexts are adaptive because they convey information. For recipients, meaning results from the integration of information from the signal and the social context. As a result, communication in animals – particularly in long-lived, social species where the same individuals interact repeatedly – constitutes a rich system of pragmatic inference in which the meaning of a communicative event depends on perception, memory and social knowledge. In the human lineage, pragmatics served as a precursor to the later evolution of semantics and syntax. Among primates, there is a striking difference in flexibility between constrained call production and more flexible perception and cognition. However, call production is more flexible in the wild, where it is affected by contextual cues, than in laboratory studies where contextual cues have been removed. Monkeys and apes may overcome the limits of constrained vocal production by producing composite signals in the same and different modalities.
In little over two decades, researchers have moved from a situation in which most studies of terrestrial mammal vocal signals focused on conspicuous characteristics, such as their rate of occurrence, and where the spectral acoustic variation was largely ignored or poorly quantified, to a field of study in which there is a much better understanding of the nature and function of the acoustic parameters that compose vocalizations. The source-filter theory, originally developed for the analysis of speech signals, has played a large role in this progress. Understanding how the acoustic variability of vocalizations is grounded within their mechanism of production has enabled researchers to predict the type of information that vocal signals are likely to contain, and to predict their co-variation with morphological and/or physiological attributes of callers. Moreover, the powerful theoretical platform derived from the source-filter theory not just conceptually supports the formulation of multilevel hypotheses, but also paves the way to develop the corresponding methodologies needed to address them. Although the full range of acoustic diversity of terrestrial mammal signals has yet to be explored, this chapter draws together a wealth of research conducted over the last two decades, and describes how source- and filter-related acoustic components encode functionally relevant information in the vocal communication systems of terrestrial mammal and how selection pressures have led to the evolution of anatomical innovations that enable animals to produce exaggerated vocal traits.
Vocal production is a central topic in biological and evolutionary approaches to animal communication, linking physics, physiology, and anatomy, on the one hand, with perception, neural processing, and evolution of communication signals, on the other. Understanding of vertebrate vocal production has increased greatly in the last two decades, mainly by building on an understanding of the physics and physiology of human vocal production initially developed by speech scientists. There is an increasing feeling among specialists in bioacoustics that this discipline has entered a new scientific era where the broad theoretical and physical underpinnings of vocal production, in a wide variety of vertebrate species, are solid and well-understood. Unfortunately, the origins of this understanding in speech science pose a problem for many nonspecialists, as the founding texts are highly technical and mathematical treatments written by and for engineers. This chapter, like the volume of which it is part, aims to provide a nontechnical introduction and overview of vertebrate vocal production written by and for biologists interested in vocal communication. The chapter provides a historical overview of the origins of two critical bodies of theory, the source-filter theory of vocal production and the myo-elastic aerodynamic theory of the voice source, and details how these theories were gradually applied to nonhuman animal vocalizations. The chapter ends with a summary of the rest of the chapters in the volume.
This chapter discusses the skulls of seven different species of marine mammals: the manatee, the harbor seal, the California sea lion, the north Atlantic right whale, the bottlenose dolphin, the polar bear, and the sea otter. These marine mammal species were chosen, in part, because much is known about them and they illustrate a wide range of morphological adaptations. The skull acts as a mechanical foundation for the fat, muscle, skin, vascular, and sensory structures that form the head. Thus, the skull alone does not dictate the contours of the head. The specific characteristics of a skull often reflect the animal's methods of feeding. Typically, the labial surface of the dentary has small openings at its rostral end for the blood vessels and nerves of the chin; manatee mental foramina are relatively large. Bony features are morphological characters or landmarks that make up one or more bones. Size, shape, and positions of bony features reflect evolutionary, developmental, and mechanical pressures in a grossly visible manner. In all vertebrates, the skull bones develop from ossification centers in a basic pattern that partially or completely encloses the brain and encapsulates the sensory organs of olfaction, vision, hearing, and balance. Skull bones can meet in several ways and attach to each other by more than one type of material. The development of the skull bones proceeds at a pace different from that of the soft tissues of the head. Bone is constantly being remodeled; this takes place at the level of the individual during its lifetime in response to trauma, nutrition, and localized conditions. The cranial cavity houses the brain, its meninges, and its vasculature. The roof and lateral walls of the braincase are typically made up of the frontal and parietal bones with the caudal wall formed by the supraoccipital and exoccipitals. Telescoping is a process often discussed when describing the skulls of cetaceans. It refers to the elongation of the rostral elements and the dorsorostral movement of caudal elements.
Although the type of information conveyed by animal vocalizations has been a focus of theoretical interest for many years, little attention has been paid to the ways in which the evolution of signals may be constrained by basic acoustics combined with functional morphology. It has been shown recently that correlations between body size and vocal tract length, combined with the causal relationship of vocal tract length to vocal tract resonances or "formants", lead to accurate acoustic correlates of body size in some mammals. In this paper, an analysis of the relationship between body size (both weight and length) and vocal tract length (measured from museum skulls) in a variety of mammalian species shows that these relationships are typical of a much wider variety of species. Strong allometric relationships between these variables are documented, both intra- and inter-specifically. An analysis of regression coefficients indicates that inter- and intra-specific relationships can be significantly different, with interspecific correlations corresponding closely to the 3.0 slope predicted by geometric isometry, but intraspecific relationships deviating significantly from it. The data suggest that the acoustic correlates of vocal tract length, formant frequencies, could provide a cue to body size in a wide variety of mammals.
The goal of this book is to inform a broad readership about a variety of measures and estimators of effect sizes for research, their proper applications and interpretations, and their limitations. Its focus is on analyzing post-research results. The book provides an evenhanded account of controversial issues in the field, such as the role of significance testing. Consistent with the trend toward greater use of robust statistical methods, the book pays much attention to the statistical assumptions of the methods and to robust measures of effect size.
Body weight, length, and vocal tract length were measured for 23 rhesus macaques (Macaca mulatta) of various sizes using radiographs and computer graphic techniques. linear predictive coding analysis of tape-recorded threat vocalizations were used to determine vocal tract resonance frequencies ("formants") for the same animals. A new acoustic variable is proposed, "formant dispersion," which should theoretically depend upon vocal tract length. Formant dispersion is the averaged difference between successive formant frequencies, and was found to be closely tied to both vocal tract length and body size. Despite the common claim that voice fundamental frequency (F0) provides an acoustic indication of body size, repeated investigations have failed to support such a relationship in many vertebrate species including humans. Formant dispersion, unlike voice pitch, is proposed to be a reliable predictor of body size in macaques, and probably many other species.
In simple linear regression analysis, measurement error in the explanatory variable causes the ordinary least‐squares estimator of the regression parameter to be biased towards zero.However, in multiple linear regression, it is shown that the assumption of measurement error in the explanatory variables does not always cause regression parameters to be biased towards zero. The direction of the bias is found to depend on the degree of orthogonality between the explanatory variables.
The northern elephant seal breeds on islands off the coast of Mexico and California. It is a highly vocal species and during the breeding season vocalization plays an important role in the maintenance of the species' highly polygynous social organization. The importance of vocalization in this species is demonstrated by the presence in the adult male of a highly modified proboscis which appears to have no function other than the production of vocal threats.Observation of colour-marked individuals on San Nicolas Island, California, showed that females of a harem tend to remain in a given spot. Females of low dominance are often forced to move by the aggressive behaviour of more dominant females and their pups are likely to become lost and to be bitten by other females. The voice of the pup attracts the mother and stimulates the mother to suckle the pup.Observations in the field combined with spectrographic analysis of tape recordings reveal two main communicational and structural classes of vocalization, attraction calls and threat sounds. Attraction sounds (mother to pup) are unpulsed, of high and variable pitch, and show clear harmonic structure. Threat sounds (both female and male) have an opposite type of structure; they are highly pulsed, of low and steady pitch, are harsh, and lack clearcut harmonics. In general, pulse interval in the threat sounds tends to increase with body size. Among males, the resonance and volume of the clap-threat increases with the size and development of the proboscis.Hissing occurs in many tetrapods and probably preceded and facilitated the evolution of vocal cords and patterned sounds; in turn the extensive use of different sounds as a means of communication probably facilitated the evolution of social life in the vertebrates. It is of interest that yearlings use the hiss as a threat and some yearling threat sounds are structurally intermediate between a hiss and the common roaring type of threat.
Acoustic communication range estimates for four northern elephant seal ( Mirounga angustirostris ) vocalization types are presented for this species. Maximum signal detection ranges are determined using an integrated approach involving: é eld measurements of vocalization source levels and spectral characteristics, signal directivity patterns, natural ambient noise measurements, and pre- viously collected laboratory audiometric data. Sig- nals and masking noise were analyzed using two é lter bandwidths believed to approximate the upper and lower limit of auditory é lter widths for the northern elephant seal auditory system. Signal de- tection ranges are estimated for representative pup ' female attraction calls' (FAC), adult female ' pup attraction calls' (PAC), adult female ' threat calls' (AFT), and adult male ' clap threat calls' (AMCT) in each of three intensity categories for biotic noise, wave noise, and wind noise. Signal detection ranges in these nine natural masking noise conditions vary from 5- 70 m for FAC, 10- 105 m for PAC, 41- 479 m for AFT, and 59- 507 m for AMCT. The results demonstrate the extent to which communi- cation ranges in the é eld can vary depending on call type, signal directivity, ambient noise conditions, and receiver capabilities. These data are also useful in considering natural constraints on acoustic com- munication in northern elephant seals, selective pressures on signal production and reception systems, and potential negative e Vects of anthropo- genic noise.