Quality prevails over identity in the sexually selected vocalisations of an ageing mammal

Background

Male sexually selected vocalisations generally contain both individuality and quality cues that are crucial in intra- as well as inter-sexual communication. As individuality is a fixed feature whereas male phenotypic quality changes with age, individuality and quality cues may be subjected to different selection pressures over time. Individuality (for example, morphology of the vocal apparatus) and quality (for example, body size and dominance status) can both affect the vocal production mechanism, inducing the same components of vocalisations to convey both kinds of information. In this case, do quality-related changes to the acoustic structure of calls induce a modification of vocal cues to identity from year to year? We investigated this question in fallow deer (Dama dama), in which some acoustic parameters of vocalisations (groans) code for both individuality and quality.

Results

We carried out a longitudinal analysis of groan individuality, examining the effects of age and dominance rank on the acoustic structure of groans of the same males recorded during consecutive years. We found both age- and rank-related changes to groans; the minimum values of the highest formant frequencies and the fundamental frequency increased with the age of males and they decreased when males became more dominant. Both age- and rank-related acoustic parameters contributed to individuality. Male quality changed with age, inducing a change in quality-related parameters and thus, a modification of vocal cues to male individuality between years.

Conclusions

The encoding of individuality and quality information in the same components of vocalisations induces a tradeoff between these two kinds of signals over time. Fallow deer vocalisations are honest signals of quality that are not fixed over time but are modified dynamically according to male quality. As they are more reliable cues to quality than to individuality, they may not be used by conspecifics to recognize a given male from one year to another, but potentially used by both sexes to assess male quality during each breeding season.

     

Rookognise: Acoustic detection and identification of individual rooks in field recordings using multi-task neural networks

Individual-level monitoring is essential in many behavioural and bioacoustics studies. Collecting and annotating those data is costly in terms of human effort, but necessary prior to conducting analysis. In particular, many studies on bird vocalisations also involve manipulating the animals or human presence during observations, which may bias vocal production. Autonomous recording units can be used to collect large amounts of data without human supervision, largely removing those sources of bias. Deep learning can further facilitate the annotation of large amounts of data, for instance to detect vocalisations, identify the species, or recognise the vocalisation types in recordings. Acoustic individual identification, however, has so far largely remained limited to a single vocalisation type for a given species. This has limited the use of those techniques for automated data collection on raw recordings, where many individuals can produce vocalisations of varying complexity, potentially overlapping one another, with the additional presence of unknown and varying background noise. This paper aims at bridging this gap by developing a system to identify individual animals in those difficult conditions. Our system leverages a combination of multi-scale information integration, multi-channel audio and multi-task learning. The multi-task learning paradigm is based the overall task into four sub-tasks, three of which are auxiliary tasks: the detection and segmentation of vocalisations against other noises, the classification of individuals vocalising at any point during a sample, and the sexing of detected vocalisations. The fourth task is the overall identification of individuals. To test our approach, we recorded a captive group of rooks, a Eurasian social corvid with a diverse vocal repertoire. We used a multi-microphone array and collected a large scale dataset of time-stamped and identified vocalisations recorded, and found the system to work reliably for the defined tasks. To our knowledge, the system is the first to acoustically identify individuals regardless of the vocalisation produced. Our system can readily assist data collection and individual monitoring of groups of animals in both outdoor and indoor settings, even across long periods of time, and regardless of a species’ vocal complexity. All data and code used in this article is available online.     

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.     

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.     

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.     

Temporal and environmental influences on the vocal behaviour of a nocturnal bird

Temporal and environmental variation in vocal activity can provide information on avian behaviour and call function not available to short‐term experimental studies. Inter‐sexual differences in this variation can provide insight into selection effects. Yet factors influencing vocal behaviour have not been assessed in many birds, even those monitored by acoustic methods. This applies to the New Zealand kiwi (Apterygidae), for which call censuses are used extensively in conservation monitoring, yet which have poorly understood acoustic ecology. We investigated little spotted kiwi Apteryx owenii vocal behaviour over 3 yr, measuring influences on vocal activity in both sexes from time of night, season, weather conditions and lunar cycle. We tested hypotheses that call rate variation reflects call function, foraging efficiency, historic predation risk and variability in sound transmission, and that there are inter‐sexual differences in call function. Significant seasonal variation showed that vocalisations were important in kiwi reproduction, and inter‐sexual synchronisation of call rates indicated that contact, pair‐bonding or resource defence were key functions. All weather variables significantly affected call rates, with elevated calling during increased humidity and ground moisture indicating a relation between vocal activity and foraging conditions. A significant decrease in calling activity on cloudy nights, combined with no moonlight effect, suggests an impact of light pollution in this species. These influences on vocal activity provide insight into kiwi call function, have direct consequences for conservation monitoring of kiwi, and have wider implications in understanding vocal behaviour in a range of nocturnal birds.     

Social associations and vocal communication in wild and captive male savannah elephants Loxodonta africana

相似文献   

The Acoustic Structure and Information Content of Female Koala Vocal Signals

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

Genetic structure in a montane ranid frog: restricted gene flow and nuclear-mitochondrial discordance

There is substantial debate over the criteria that should be used to group populations of a species into distinct units for conservation (e.g. evolutionarily significant units, management units, distinct population segments). However, in practice molecular genetic differentiation is often the only or main criterion used to identify such units. Most genetic studies attempting to define conservation units in animals use a single molecular marker, most often mitochondrial, and use samples from a limited number of populations throughout the species' range. Although there are many benefits to using mtDNA, certain features can cause it to show patterns of differentiation among populations that do not reflect the history of differentiation at the nuclear genome where loci controlling traits of adaptive significance presumably occur. Here we illustrate an example of such mitochondrial-nuclear discordance in a ranid frog, and show how using mtDNA or nuclear loci alone could have led to very different conservation recommendations. We also found very high genetic differentiation among populations on a local scale, and discuss the conservation implications of our results.     

Perception of male caller identity in Koalas (Phascolarctos cinereus): acoustic analysis and playback experiments

The ability to signal individual identity using vocal signals and distinguish between conspecifics based on vocal cues is important in several mammal species. Furthermore, it can be important for receivers to differentiate between callers in reproductive contexts. In this study, we used acoustic analyses to determine whether male koala bellows are individually distinctive and to investigate the relative importance of different acoustic features for coding individuality. We then used a habituation-discrimination paradigm to investigate whether koalas discriminate between the bellow vocalisations of different male callers. Our results show that male koala bellows are highly individualized, and indicate that cues related to vocal tract filtering contribute the most to vocal identity. In addition, we found that male and female koalas habituated to the bellows of a specific male showed a significant dishabituation when they were presented with bellows from a novel male. The significant reduction in behavioural response to a final rehabituation playback shows this was not a chance rebound in response levels. Our findings indicate that male koala bellows are highly individually distinctive and that the identity of male callers is functionally relevant to male and female koalas during the breeding season. We go on to discuss the biological relevance of signalling identity in this species' sexual communication and the potential practical implications of our findings for acoustic monitoring of male population levels.     

NEWS

ABSTRACT

Australian fur seals Arctocephalus pusillus doriferus are colonial breeding animals forming dense social groups during the breeding season. During this time, males establish and defend territories through physical conflicts, stereotyped posturing and vocalisations. While vocalisations are suggested to play an important role in male recognition systems, it has received little attention. Recordings of nine adult male Australian fur seals were made during the 2000 and 2001 breeding seasons at Kanowna Island (39° 10′S, 146° 18′ E), Bass Strait, Australia. The in-air bark vocalisations of territory-holding males were used to characterise the Bark Call and to determine whether males produce individually distinct calls, which could be used as a basis for vocal recognition. Seventeen frequency and temporal variables were measured from a total of 162 barks from nine individual males. The Bark Series was more reliably classified (83%) to the correct caller compared to the Bark Unit. This was assigned with less certainty (68%), although the classification was still relatively high. Findings from this study indicate that there is sufficient stereotypy within individual calls, and sufficient variation between them, to enable vocal recognition in male Australian fur seals.     

BIOACOUSTIC PUBLICATIONS, 1989

ABSTRACT

In order to increase understanding of African elephant vocal communication and to standardise the terminology used to describe vocalisations, this study examined acoustic and temporal characteristics of 983 vocalisations from 2 male and 6 female captive African elephants. Recording collars were used to monitor vocalisations and videotape to simultaneously record behaviour, allowing for unambiguous attribution of sounds to individuals, even in close proximity. Eight acoustically distinct categories of calls were defined in terms of structural characteristics; two of these categories are described for the first time. Low-frequency vocalisations containing infrasonic components were predominant in this localised communication context and showed a gradation of variation in acoustic structure and duration. Most calls were part of temporally closed exchanges between individuals and coincided with short-distance interactions. In addition, male-female choruses and non-musth rumbles from males were documented, suggesting that the African elephant vocal repertoire may be more complex than previously reported.     

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.     

Conservation of the Eurasian beaver Castor fiber: an olfactory perspective

• 1 Chemical communication in mammals includes an array of specific behaviours that are often ignored in terms of their potential relevance to conservation. Often used during territorial or social interactions between animals, chemical communication can also be used as a tool in reintroduction programmes. Reintroductions still exhibit high failure rates and methods to improve success should be investigated. The Eurasian beaver Castor fiber has been widely reintroduced across Europe after its near extinction in the 19th century.
• 2 Using olfactory studies in the beaver, we aim to demonstrate how scent transfers a range of information about the sender which can be used to monitor social and territorial behaviour along with general well‐being. Scent manipulation can be used to reduce human–beaver conflicts, and aid reintroduction success through reducing stress and territorial conflicts, and by influencing dispersal and settlement.
• 3 Two species of beavers, the Eurasian beaver and the North American beaver Castor canadensis, occupy freshwater habitats throughout North America and in parts of South America, most of Europe and parts of Asia. Most of the reviewed literature concerns the wild Eurasian beaver, its chemical communication and conservation; however, captive studies and those addressing North American beavers are also included.
• 4 Chemical communication is advanced and has been well documented in this highly territorial species. However, few studies directly link olfaction with conservation practices.
• 5 Olfactory studies in beavers can provide non‐invasive methods to monitor translocated animals and indicators of health. We conclude that chemical analysis, olfactory studies and behavioural manipulations involving semiochemicals have important impacts on conservation and can generate practical solutions to conservation problems including aiding animal capture, captive stress reduction, breeding pair formation and release site fidelity.

     

Learned Vocal Variation Is Associated with Abrupt Cryptic Genetic Change in a Parrot Species Complex

Contact zones between subspecies or closely related species offer valuable insights into speciation processes. A typical feature of such zones is the presence of clinal variation in multiple traits. The nature of these traits and the concordance among clines are expected to influence whether and how quickly speciation will proceed. Learned signals, such as vocalizations in species having vocal learning (e.g. humans, many birds, bats and cetaceans), can exhibit rapid change and may accelerate reproductive isolation between populations. Therefore, particularly strong concordance among clines in learned signals and population genetic structure may be expected, even among continuous populations in the early stages of speciation. However, empirical evidence for this pattern is often limited because differences in vocalisations between populations are driven by habitat differences or have evolved in allopatry. We tested for this pattern in a unique system where we may be able to separate effects of habitat and evolutionary history. We studied geographic variation in the vocalizations of the crimson rosella (Platycercus elegans) parrot species complex. Parrots are well known for their life-long vocal learning and cognitive abilities. We analysed contact calls across a ca 1300 km transect encompassing populations that differed in neutral genetic markers and plumage colour. We found steep clinal changes in two acoustic variables (fundamental frequency and peak frequency position). The positions of the two clines in vocal traits were concordant with a steep cline in microsatellite-based genetic variation, but were discordant with the steep clines in mtDNA, plumage and habitat. Our study provides new evidence that vocal variation, in a species with vocal learning, can coincide with areas of restricted gene flow across geographically continuous populations. Our results suggest that traits that evolve culturally can be strongly associated with reduced gene flow between populations, and therefore may promote speciation, even in the absence of other barriers.     

Estimating Orangutan Densities Using the Standing Crop and Marked Nest Count Methods: Lessons Learned for Conservation

Reliable estimates of great ape abundance are needed to assess distribution, monitor population status, evaluate conservation tactics, and identify priority populations for conservation. Rather than using direct counts, surveyors often count ape nests. The standing crop nest count (SCNC) method converts the standing stock of nests into animal densities using a set of parameters, including nest decay rate. Nest decay rates vary greatly over space and time, and it takes months to calculate a site-specific value. The marked nest count (MNC) method circumvents this issue and only counts new nests produced during a defined period. We compared orangutan densities calculated by the two methods using data from studies in Sumatra and Kalimantan, Indonesia. We show how animal densities calculated using nest counts should be cautiously interpreted when used to make decisions about management or budget allocation. Even with site-specific decay rates, short studies using the SCNC method may not accurately reflect the current population unless conducted at a scale sufficient to include wide-ranging orangutan movement. Density estimates from short studies using the MNC method were affected by small sample sizes and by orangutan movement. To produce reliable results, the MNC method may require a similar amount of effort as the SCNC method. We suggest a reduced reliance on the traditional line transect surveys in favor of feasible alternative methods when absolute abundance numbers are not necessary or when site-specific nest decay rates are not known. Given funding constraints, aerial surveys, reconnaissance walks, and interview techniques may be more cost-effective means of accomplishing some survey goals.     

Measuring vertebrate telomeres: applications and limitations

Telomeres are short tandem repeated sequences of DNA found at the ends of eukaryotic chromosomes that function in stabilizing chromosomal end integrity. In vivo studies of somatic tissue of mammals and birds have shown a correlation between telomere length and organismal age within species, and correlations between telomere shortening rate and lifespan among species. This result presents the tantalizing possibility that telomere length could be used to provide much needed information on age, ageing and survival in natural populations where longitudinal studies are lacking. Here we review methods available for measuring telomere length and discuss the potential uses and limitations of telomeres as age and ageing estimators in the fields of vertebrate ecology, evolution and conservation.     

Subharmonics increase the auditory impact of female koala rejection calls

Although non‐linear phenomena are common in human and non‐human animal vocalisations, their functional relevance remains poorly understood. One theory posits that non‐linear phenomena generate unpredictability in vocalisations, which increases the auditory impact of vocal signals, and makes animals less likely to habituate to call repetition. Female koalas (Phascolarctos cinereus) produce vocal signals when they reject male copulation attempts that contain relatively high levels of non‐linear phenomena, and thus may function as attention grabbing vocal signals during the breeding season. To test this hypothesis, we used playback experiments: firstly, to determine whether female rejection calls induce heightened behavioural responses in free‐ranging male koalas during the breeding season, and secondly, to examine how the relative amount of non‐linear phenomena in rejection calls influences male behavioural response. The results show that male koalas look for longer towards speakers broadcasting playback sequences of male bellows followed by a series of female rejection calls than those broadcasting only male bellows. In addition, female rejection call sequences with more subharmonics, higher harmonics‐to‐noise ratios, and less biphonation produced the greatest male looking responses. Our findings support the hypothesis that female koala rejection calls function to grab male attention during the breeding season, and indicate that subharmonics are the main acoustic feature that increases the auditory impact of these vocal signals.