What Makes Vocalisation Frequency an Unreliable Signal of Body Size in Birds? A Study on Black Swans

In many animal species, the frequency (pitch) of vocalisations correlates negatively with body size and may thus signal competitive ability. However, this relationship is absent in other species. Understanding why this difference exists across species may help to explain some of the diversity of vocal communication systems. We assessed whether vocalisation frequency signals body size in black swans (Cygnus atratus), and how this is affected by (i) variation in frequency within individuals and (ii) size variation across individuals. Frequency was correlated with body size and mass, with slopes close to the allometry expected if the birds were maximising sound radiation, but the explained variation in frequency was low. Within‐individual variation in vocalisation frequency was greater in male than female swans, and the reliability of frequency as a signal of size in males was correspondingly lower. A review of the literature on the relationship between the frequency of avian vocalisations and body size also showed smaller effect sizes for more variable vocalisations (birdsongs), than for simpler vocalisations. Vocalisation frequency was more reliably correlated with body size when the sexes were pooled (creating a larger range of variation in size) than when the relationship was examined for either sex separately, although male and female data followed the same allometric line. These results show that variation in frequency within individuals and low variation in size across individuals reduce the reliability of vocalisation frequency as a signal of body size, which helps to understand differences among species in the signal value of vocalisation frequency.     

Automatic recording of individual oestrus vocalisation in group-housed dairy cattle: development of a cattle call monitor

Oestrus detection remains a problem in the dairy cattle industry. Therefore, automatic detection systems have been developed to detect specific behavioural changes at oestrus. Vocal behaviour has not been considered in such automatic oestrus detection systems in cattle, though the vocalisation rate is known to increase during oestrus. The main challenge in using vocalisation to detect oestrus is correctly identifying the calling individual when animals are moving freely in large groups, as oestrus needs to be detected at an individual level. Therefore, we aimed to automate vocalisation recording and caller identification in group-housed dairy cows. This paper first presents the details of such a system and then presents the results of a pilot study validating its functionality, in which the automatic detection of calls from individual heifers was compared to video-based assessment of these calls by a trained human observer, a technique that has, until now, been considered the ‘gold standard’. We developed a collar-based cattle call monitor (CCM) with structure-borne and airborne sound microphones and a recording unit and developed a postprocessing algorithm to identify the caller by matching the information from both microphones. Five group-housed heifers, each in the perioestrus or oestrus period, were equipped with a CCM prototype for 5 days. The recorded audio data were subsequently analysed and compared with audiovisual recordings. Overall, 1404 vocalisations from the focus heifers and 721 vocalisations from group mates were obtained. Vocalisations during collar changes or malfunctions of the CCM were omitted from the evaluation. The results showed that the CCM had a sensitivity of 87% and a specificity of 94%. The negative and positive predictive values were 80% and 96%, respectively. These results show that the detection of individual vocalisations and the correct identification of callers are possible, even in freely moving group-housed cattle. The results are promising for the future use of vocalisation in automatic oestrus detection systems.     

Vocal individuality of large-tailed nightjar (Caprimulgus macrurus) in Peninsular Malaysia

All four nightjar species resident in Peninsular Malaysia are vocally distinct, yet they remain little studied. Conventional field methods based on visual cues to study diurnal species may be impractical for nightjars. Alternatively, aural survey can potentially be applied on nightjars provided that individuality in their vocalisations can be proven. Our study aimed to determine the vocal individuality of the common, large-tailed nightjar (Caprimulgus macrurus) in oil palm smallholdings and an isolated forest patch located in Selangor, Peninsular Malaysia. From the call recordings obtained from 22 individuals, results of the Kruskal-Wallis analysis revealed significant differences in all the nine vocal parameters (call length, interquartile range bandwidth, low, high, average, centre and peak frequencies as well as first and third quartile frequencies) measured among individual nightjars (p < 0.001) regardless of study sites. Discriminant Function Analysis showed that more than 94.5% of original grouped cases were correctly classified. This implied that the majority of vocalizations can be assigned to individual birds based on the parameters measured. This study demonstrated the occurrence of vocal individuality in the large-tailed nightjar and such a finding pertaining to distinct vocalisations at the individual level will compensate for the limited access to visual cues in field surveys, as with the case for all nocturnal birds.     

The role of vocal individuality in conservation

Identifying the individuals within a population can generate information on life history parameters, generate input data for conservation models, and highlight behavioural traits that may affect management decisions and error or bias within census methods. Individual animals can be discriminated by features of their vocalisations. This vocal individuality can be utilised as an alternative marking technique in situations where the marks are difficult to detect or animals are sensitive to disturbance. Vocal individuality can also be used in cases were the capture and handling of an animal is either logistically or ethically problematic. Many studies have suggested that vocal individuality can be used to count and monitor populations over time; however, few have explicitly tested the method in this role. In this review we discuss methods for extracting individuality information from vocalisations and techniques for using this to count and monitor populations over time. We present case studies in birds where vocal individuality has been applied to conservation and we discuss its role in mammals.     

Avian vocal mimicry: a unified conceptual framework

Mimicry is a classical example of adaptive signal design. Here, we review the current state of research into vocal mimicry in birds. Avian vocal mimicry is a conspicuous and often spectacular form of animal communication, occurring in many distantly related species. However, the proximate and ultimate causes of vocal mimicry are poorly understood. In the first part of this review, we argue that progress has been impeded by conceptual confusion over what constitutes vocal mimicry. We propose a modified version of Vane‐Wright's (1980) widely used definition of mimicry. According to our definition, a vocalisation is mimetic if the behaviour of the receiver changes after perceiving the acoustic resemblance between the mimic and the model, and the behavioural change confers a selective advantage on the mimic. Mimicry is therefore specifically a functional concept where the resemblance between heterospecific sounds is a target of selection. It is distinct from other forms of vocal resemblance including those that are the result of chance or common ancestry, and those that have emerged as a by‐product of other processes such as ecological convergence and selection for large song‐type repertoires. Thus, our definition provides a general and functionally coherent framework for determining what constitutes vocal mimicry, and takes account of the diversity of vocalisations that incorporate heterospecific sounds. In the second part we assess and revise hypotheses for the evolution of avian vocal mimicry in the light of our new definition. Most of the current evidence is anecdotal, but the diverse contexts and acoustic structures of putative vocal mimicry suggest that mimicry has multiple functions across and within species. There is strong experimental evidence that vocal mimicry can be deceptive, and can facilitate parasitic interactions. There is also increasing support for the use of vocal mimicry in predator defence, although the mechanisms are unclear. Less progress has been made in explaining why many birds incorporate heterospecific sounds into their sexual displays, and in determining whether these vocalisations are functionally mimetic or by‐products of sexual selection for other traits such as repertoire size. Overall, this discussion reveals a more central role for vocal mimicry in the behavioural ecology of birds than has previously been appreciated. The final part of this review identifies important areas for future research. Detailed empirical data are needed on individual species, including on the structure of mimetic signals, the contexts in which mimicry is produced, how mimicry is acquired, and the ecological relationships between mimic, model and receiver. At present, there is little information and no consensus about the various costs of vocal mimicry for the protagonists in the mimicry complex. The diversity and complexity of vocal mimicry in birds raises important questions for the study of animal communication and challenges our view of the nature of mimicry itself. Therefore, a better understanding of avian vocal mimicry is essential if we are to account fully for the diversity of animal signals.     

Social vocal communication in captive Pacific walruses Odobenus rosmarus divergens

Walrus are highly gregarious pinnipeds that can form herds of several hundreds or thousands of individuals when hauling out on ice or on land. They produce vocalisations in almost all social interactions, from aggressive vocalisations, contact calls involved in mother–calf bond to adult–adult communication to stereotyped courtship display during the mating season. The knowledge on walrus’ vocal behaviour and its perceptual abilities is limited due to the extreme difficulty of studying these animals in their natural environment. In the present study, we reported the results of a pilot experimental work on group/social vocal communication in captive Pacific Walruses (Odobenus rosmarus divergens). By analysing the main vocalisations produced by females and males during social interactions, we found some differences in their call characteristics compared to the Atlantic subspecies. In a second step, we experimentally demonstrated the abilities of females and mature males to discriminate between vocalizations of individuals from their own group and those of unknown individuals. In spite of the low sample size of animals, these findings on captive walruses improved knowledge of the cognitive abilities of this endemic Arctic species.     

Vocalisations of wild common marmosets are influenced by diurnal and ontogenetic factors

The vocalisations of wild common marmosets, Callithrix jacchus, were recorded to investigate whether call rate by individuals is affected by time of day, age, sex or dominance rank within a group. We also investigated how vocalisation pitch was affected by age, focussing on a single common call, the trill call. Adults vocalised more than juveniles or infants during the majority of daylight hours. Only the call rate of juveniles varied significantly over the day. No differences were found between either sex or dominance rank with respect to rate of vocalisations. The trill calls emitted by young wild common marmosets were of a higher pitch than those emitted by adults. We conclude that the auditory communication of wild common marmosets is related to the age of the animals, both in terms of call rate and the physical characteristics of their vocalisations.     

Assessing bird vocalisation identification accuracy using a computer-based quiz

Reliable information on bird population trends is required to inform management and policy decisions. The ability to accurately identify species is therefore essential, yet there have been few studies on this subject. This study investigated accuracy of bird vocalisation identification via the use of a computer-based quiz, to provide data on difficult-to-identify species which may be used to inform training requirements and data analyses. Identification accuracy was highly variable, and for several species some vocalisation types were more difficult to identify accurately than others. Analysis of incorrect responses revealed that confusion was usually between species with similar vocalisations. A comparison of participants’ perceived identification ability (via self-assessment) to their actual ability, as determined from their quiz score showed that advanced participants usually assessed their ability accurately, whilst the remaining participants (intermediate, novice and no experience) generally underestimated their ability, demonstrating the need for an objective means of bird identification skill assessment.     

BIOACOUSTIC PUBLICATIONS, 1988

ABSTRACT

We examined vocalisations of a solitary subterranean rodent, the Silvery Mole-rat Heliophobius argenteocinereus (Bathyergidae). Seven true vocalisations and one mechanical vocalisation were identified. The main frequencies of the analysed sounds (0.34–13.17 kHz) match to a great extent the frequency range suitable for transmission in underground burrows. Due to the narrow frequency range of vocalisations, motivation is predominantly expressed by the rate of tonality rather than by frequency changes. The vocal repertoire of the Silvery Mole-rat perfectly matches to Morton's MS rules, i.e. that low-frequency and harsh vocalisations indicate hostility whereas high tonal calls signalise appeasement or fear. In comparison with social species, this solitary bathyergid produces fewer calls. It lacks contact and alarm calls, but has a rich repertoire of mating calls (mating ends with duet vocalization of male and female). Acoustic signals seem to play a major role in lowering natural aggressiveness during the mating period.     

Rapid Onset of Maternal Vocal Recognition in a Colonially Breeding Mammal,the Australian Sea Lion

Background

In many gregarious mammals, mothers and offspring have developed the abilities to recognise each other using acoustic signals. Such capacity may develop at different rates after birth/parturition, varying between species and between the participants, i.e., mothers and young. Differences in selective pressures between species, and between mothers and offspring, are likely to drive the timing of the onset of mother-young recognition. We tested the ability of Australian sea lion mothers to identify their offspring by vocalisation, and examined the onset of this behaviour in these females. We hypothesise that a rapid onset of recognition may reflect an adaptation to a colonial lifestyle.

Principal Findings

In a playback study maternal responses to own pup and non-filial vocalisations were compared at 12, 24 and every subsequent 24 hours until the females'' first departure post-partum. Mothers showed a clear ability to recognise their pup''s voice by 48 hours of age. At 24 hours mothers called more, at 48 hours they called sooner and at 72 hours they looked sooner in response to their own pup''s vocalisations compared to those of non-filial pups.

Conclusions

We demonstrate that Australian sea lion females can vocally identify offspring within two days of birth and before mothers leave to forage post-partum. We suggest that this rapid onset is a result of selection pressures imposed by a colonial lifestyle and may be seen in other colonial vertebrates. This is the first demonstration of the timing of the onset of maternal vocal recognition in a pinniped species.     

Individual Variation in Behavioural Reactions to Unfamiliar Conspecific Vocalisation and Hormonal Underpinnings in Male Chimpanzees

It has been established that various species exhibit personality, defined as intra‐individual consistency and inter‐individual variation in behavioural phenotypes. For example, certain individuals may demonstrate consistently greater behavioural reactions and elevated stress responses. We conducted playback experiments and hormonal analyses on male chimpanzees (Pan troglodytes) in captivity to investigate the patterns and proximate mediators of individual variations in behavioural reactions. We found intra‐individual consistency and inter‐individual variation in behavioural reactions (intensive vigilance towards the direction of speakers) to vocalisations by unfamiliar chimpanzees. This behavioural reaction was positively correlated with changes in salivary cortisol concentration, suggesting that stress is a proximate factor mediating the variation in behavioural reactions. The males who were highly responsive to the conspecific vocalisation also exhibited high behavioural reactions towards the neutral broadcast stimulus (the jungle crow’s Corvus macrorhynchos ‘ka’ vocalisation). This observation is consistent with the notion that male chimpanzees vary in intrinsic behavioural tendency to different stimuli.     

Ecological inferences about marine mammals from passive acoustic data

Monitoring on the basis of sound recordings, or passive acoustic monitoring, can complement or serve as an alternative to real-time visual or aural monitoring of marine mammals and other animals by human observers. Passive acoustic data can support the estimation of common, individual-level ecological metrics, such as presence, detection-weighted occupancy, abundance and density, population viability and structure, and behaviour. Passive acoustic data also can support estimation of some community-level metrics, such as species richness and composition. The feasibility of estimation and certainty of estimates is highly context dependent, and understanding the factors that affect the reliability of measurements is useful for those considering whether to use passive acoustic data. Here, we review basic concepts and methods of passive acoustic sampling in marine systems that often are applicable to marine mammal research and conservation. Our ultimate aim is to facilitate collaboration among ecologists, bioacousticians, and data analysts. Ecological applications of passive acoustics require one to make decisions about sampling design, which in turn requires consideration of sound propagation, sampling of signals, and data storage. One also must make decisions about signal detection and classification and evaluation of the performance of algorithms for these tasks. Investment in the research and development of systems that automate detection and classification, including machine learning, are increasing. Passive acoustic monitoring is more reliable for detection of species presence than for estimation of other species-level metrics. Use of passive acoustic monitoring to distinguish among individual animals remains difficult. However, information about detection probability, vocalisation or cue rate, and relations between vocalisations and the number and behaviour of animals increases the feasibility of estimating abundance or density. Most sensor deployments are fixed in space or are sporadic, making temporal turnover in species composition more tractable to estimate than spatial turnover. Collaborations between acousticians and ecologists are most likely to be successful and rewarding when all partners critically examine and share a fundamental understanding of the target variables, sampling process, and analytical methods.     

Invited review: The evolution of cattle bioacoustics and application for advanced dairy systems

Vocalisations are commonly expressed by gregarious animals, including cattle, as a form of short- and long-distance communication. They can provide conspecifics with meaningful information about the physiology, affective state and physical attributes of the caller. In cattle, calls are individually distinct meaning they assist animals to identify specific individuals in the herd. Consequently, there is potential for these vocalisations to be acoustically analysed to make inferences about how individual animals or herds are coping with their external surroundings, and then act on these signals to improve feed conversion efficiency, reproductive efficiency and welfare. In the case of dairy farming, where herd sizes are expanding and farmers are becoming more reliant on technologies to assist in the monitoring of cattle, the study of vocal behaviour could provide an objective, cost effective and non-invasive alternative to traditional measures of welfare. The vocalisations of cattle in response to calf separation, social isolation and painful husbandry procedures, alongside changes to feeding and oestrous activity are here reviewed. For future application of sound technology, research is first necessary to analyse the acoustic structure of cattle vocalisations and determine the specific information they encode. This review draws together the latest research in field of cattle bioacoustics highlighting how the source–filter theory and affective state dimensional approach can be adopted to decode this information and improve on-farm management.     

Male Songbird Indicates Body Size with Low-Pitched Advertising Songs

Body size is a key sexually selected trait in many animal species. If size imposes a physical limit on the production of loud low-frequency sounds, then low-pitched vocalisations could act as reliable signals of body size. However, the central prediction of this hypothesis – that the pitch of vocalisations decreases with size among competing individuals – has limited support in songbirds. One reason could be that only the lowest-frequency components of vocalisations are constrained, and this may go unnoticed when vocal ranges are large. Additionally, the constraint may only be apparent in contexts when individuals are indeed advertising their size. Here we explicitly consider signal diversity and performance limits to demonstrate that body size limits song frequency in an advertising context in a songbird. We show that in purple-crowned fairy-wrens, Malurus coronatus coronatus, larger males sing lower-pitched low-frequency advertising songs. The lower frequency bound of all advertising song types also has a significant negative relationship with body size. However, the average frequency of all their advertising songs is unrelated to body size. This comparison of different approaches to the analysis demonstrates how a negative relationship between body size and song frequency can be obscured by failing to consider signal design and the concept of performance limits. Since these considerations will be important in any complex communication system, our results imply that body size constraints on low-frequency vocalisations could be more widespread than is currently recognised.     

Contact calling behaviour in the male ring‐tailed lemur (Lemur catta)

The ring‐tailed lemur (Lemur catta) is a group‐living strepsirhine primate endemic to Madagascar that has a complex vocal repertoire including affiliative moan and hmm calls. Past research has suggested that both vocalisations may be contact calls, and we assessed their usage in addition to examining the effect of individual differences and social factors on male calling behaviour. We tested three hypotheses: the group cohesion, preferred companion and individual differences hypotheses. From March to July 2010, 565 h of focal animal data were collected on 31 males aged ≥1 year at the Beza Mahafaly Special Reserve, Madagascar. Focal males were observed for 30 min, with vocalisations, allogrooming and agonistic interactions noted using one‐zero sampling, and general behaviour, nearest neighbour identity and distance noted using instantaneous point sampling, all at 2.5 min intervals. We found support for the group cohesion hypothesis for both vocalisations, and support for the preferred companion and individual differences hypotheses for the hmm but not the moan vocalisation. Moan and hmm calls maintained the distance between a male and his nearest neighbour, and were made at higher rates during behaviours which may lead to separation from conspecifics, such as travel and vigilance. Males made hmm calls at higher rates when they were low‐ranking, and/or when the nearest neighbour of a male or a preferred companion of either sex. Low‐ranking males may hmm call to maintain proximity to specific individuals within social groups who will show them increased tolerance, with the hmm signalling peaceful intent. Ring‐tailed lemurs are one of the best living models of gregarious primate ancestors, and gaining a better knowledge of the function and range of usage of their contact calls informs our understanding of the evolution of primate cognition.     

Avian vocalisations: the female perspective

Research on avian vocalisations has traditionally focused on male song produced by oscine passerines. However, accumulating evidence indicates that complex vocalisations can readily evolve outside the traditional contexts of mate attraction and territory defence by male birds, and yet the previous bias towards male song has shaped – and continues to shape – our understanding of avian communication as a whole. Accordingly, in this review we seek to address this imbalance by synthesising studies on female vocalisations from across signalling contexts throughout the Aves, and discuss the implications of recent empirical advances for our understanding of vocalisations in both sexes. This review reveals great structural and functional diversity among female vocalisations and highlights the important roles that vocalisations can play in mediating female-specific behaviours. However, fundamental gaps remain. While there are now several case studies that identify the function of female vocalisations, few quantify the associated fitness benefits. Additionally, very little is known about the role of vocal learning in the development of female vocalisations. Thus, there remains a pressing need to examine the function and development of all forms of vocalisations in female birds. In the light of what we now know about the functions and mechanisms of female vocalisations, we suggest that conventional male-biased definitions of songs and calls are inadequate for furthering our understanding of avian vocal communication more generally. Therefore, we propose two simple alternatives, both emancipated from the sex of the singer. The first distinguishes song from calls functionally as a sexually selected vocal signal, whilst the second distinguishes them mechanistically in terms of their underlying neurological processes. It is clear that more investigations are needed into the ultimate and proximate causes of female vocalisations; however, these are essential if we are to develop a holistic epistemology of avian vocal communication in both sexes, across ecological contexts and taxonomic divides.     

BIOACOUSTIC PUBLICATIONS, 1989

ABSTRACT

Coruros Spalacopus cyanus, social fossorial rodents from Chile, use a complex acoustic repertoire with eleven different true vocalisations and one mechanical sound in various behavioural contexts. The complex of contact calls is particularly well differentiated. Juvenile coruros produced six true vocalisations of which four were structurally identical to adult calls. One vocalisation had components of two adult sounds and one occurred only in juvenile animals. Certain calls from the adult repertoire were lacking. The frequencies of sounds of juveniles were considerably higher than those of adults, with many sounds reaching the ultrasonic range. Nevertheless, pure ultrasonic sounds were not recorded.

The frequencies of the analysed sounds of coruros extended from 0.17 to 20.33 kHz with dominant frequency components between 0.17 and 10 kHz. The acoustic properties of calls are suitable for transmission above and below ground, thus providing further indirect evidence that coruros are not strictly confined to an underground way of life. Indeed, the great variability of frequency ranges, with lower frequencies always being included, reflects a specialisation for communication in variable acoustic environments.

The most distinctive and unique vocalisation of coruros is the long duration musical trilling (lasting up to two minutes), which is a long-distance call emitted in alarm and arousal contexts. Recordings of this call from natural burrows in the field in Chile showed similar structural features to vocalisations from captive colonies in the laboratory.

Our findings provide a further example of matching physical properties of vocalisations to the acoustic conditions of the habitat. However, vocalisations in subterranean rodents consist almost exclusively of short-distance calls, the trilling of coruros being the notable exception. Since the selective pressure of the acoustic environment upon the evolution of short-distance vocalisations is probably minimal, we suggest that during their evolution, subterranean mammals have matched their vocalisations primarily to their hearing range and not directly to the acoustics underground. Hearing probably has been the primary target of natural selection, serving not only for communication but also for detection of predators (and, in carnivores, of prey).     

Territorial dynamics of Mexican Ant‐thrushes Formicarius moniliger revealed by individual recognition of their songs

The ability to monitor interactions between individuals over time can provide us with information on life histories, mating systems, behavioural interactions between individuals and ecological interactions with the environment. Tracking individuals over time has traditionally been a time‐ and often a cost‐intensive exercise, and certain types of animals are particularly hard to monitor. Here we use canonical discriminant analysis (CDA) to identify individual Mexican Ant‐thrushes using data extracted with a semi‐automated procedure from song recordings. We test the ability of CDA to identify individuals over time, using recordings obtained over a 4‐year period. CDA correctly identified songs of 12 individual birds 93.3% of the time from recordings in one year (2009), while including songs of 18 individuals as training data. Predicting singers in one year using recordings from other years indicated some instances of variation, with correct classification in the range of 67–88%; one individual was responsible for the great majority (66%) of classification errors. We produce temporal maps of the study plot showing that considerably more information was provided by identifying individuals from their songs than by ringing and re‐sighting colour‐ringed individuals. The spatial data show site fidelity in males, but medium‐term pair bonds and an apparently large number of female floaters. Recordings can be used to monitor intra‐ and intersexual interactions of animals, their movements over time, their interactions with the environment and their population dynamics.     

Vocal Signature in Wild Infant Chimpanzees

A large array of communication signals supports the fission/fusion social organization in chimpanzees, and among them the acoustic channel plays a large part because of their forest habitat. Adult vocalizations convey social and ecological information to their recipients allowing them to obtain cues about an ongoing event from calls only. In contrast to adult vocalizations, information encoded in infant calls had been hardly investigated. Studies mainly focused on vocal development. The present article aims at assessing the acoustic cues that support individual identity coding in infant chimpanzees. By analyzing recordings performed in the wild from seven 3‐year‐old infant chimpanzees, we showed that their calls support a well‐defined individual vocal signature relying on spectral cues. To assess the reliability of the signature across the calls of an individual, we defined two subsets of recordings on the basis of the characteristics of the frequency modulation (whimpers and screams) and showed that both call types present a reliable vocal signature. Early vocal signature may allow the mother and other individuals in the group to identify the infant caller when visual contact is broken. Chimpanzee mothers may have developed abilities to cope with changing vocal signatures while their infant, still vulnerable, gains in independence in close habitat. Am. J. Primatol. 75:324‐332, 2013. © 2012 Wiley Periodicals, Inc.