Multimodal communication and audience directedness in the greeting behaviour of semi-captive African savannah elephants.

Many species communicate by combining signals into multimodal combinations. Elephants live in multi-level societies where individuals regularly separate and reunite. Upon reunion, elephants often engage in elaborate greeting rituals, where they use vocalisations and body acts produced with different body parts and of various sensory modalities (e.g., audible, tactile). However, whether these body acts represent communicative gestures and whether elephants combine vocalisations and gestures during greeting is still unknown. Here we use separation-reunion events to explore the greeting behaviour of semi-captive elephants (Loxodonta africana). We investigate whether elephants use silent-visual, audible, and tactile gestures directing them at their audience based on their state of visual attention and how they combine these gestures with vocalisations during greeting. We show that elephants select gesture modality appropriately according to their audience's visual attention, suggesting evidence of first-order intentional communicative use. We further show that elephants integrate vocalisations and gestures into different combinations and orders. The most frequent combination consists of rumble vocalisations with ear-flapping gestures, used most often between females. By showing that a species evolutionarily distant to our own primate lineage shows sensitivity to their audience's visual attention in their gesturing and combines gestures with vocalisations, our study advances our understanding of the emergence of first-order intentionality and multimodal communication across taxa.

Sound Visualization Demonstrates Velopharyngeal Coupling and Complex Spectral Variability in Asian Elephants.

Sound production mechanisms set the parameter space available for transmitting biologically relevant information in vocal signals. Low-frequency rumbles play a crucial role in coordinating social interactions in elephants' complex fission-fusion societies. By emitting rumbles through either the oral or the three-times longer nasal vocal tract, African elephants alter their spectral shape significantly. In this study, we used an acoustic camera to visualize the sound emission of rumbles in Asian elephants, which have received far less research attention than African elephants. We recorded nine adult captive females and analyzed the spectral parameters of 203 calls, including vocal tract resonances (formants). We found that the majority of rumbles (64%) were nasally emitted, 21% orally, and 13% simultaneously through the mouth and trunk, demonstrating velopharyngeal coupling. Some of the rumbles were combined with orally emitted roars. The nasal rumbles concentrated most spectral energy in lower frequencies exhibiting two formants, whereas the oral and mixed rumbles contained higher formants, higher spectral energy concentrations and were louder. The roars were the loudest, highest and broadest in frequency. This study is the first to demonstrate velopharyngeal coupling in a non-human animal. Our findings provide a foundation for future research into the adaptive functions of the elephant acoustic variability for information coding, localizability or sound transmission, as well as vocal flexibility across species.

Sentinel behavior in captive meerkats (Suricata suricatta).

The social and cooperative behavior of meerkats (Suricata suricatta), specifically their sentinel behavior, has been intensively studied in free-ranging populations. This study focuses on whether guarding in captive meerkats exhibits a pattern similar to that described for wild groups. Sentinel behavior in captivity has been somewhat neglected because predation is usually not a critical factor. Nonetheless, observations in captivity might reveal whether individual or group experience influences this specific behavior pattern. We observed three captive meerkat groups (in outdoor as well as indoor enclosures) and analyzed the duration of guarding sequences, the number of established guards, the guard posture, and the individual guard positions. We also conducted playback experiments to investigate the reaction of the sentinel and the group to bird calls (songbird vs. predatory bird species). The results demonstrated that captive groups behave much the same as wild groups. Certain individuals performed the guard job more often than other group members. Accordingly, the "super sentinels" observed in the wild also exist in captive groups. Playbacks showed that the sentinels reacted more strongly to the calls of predatory bird species, indicating that captive meerkats are able to categorize bird calls. We also documented major differences in behavioral responses to the calls of specific predatory bird species. Our observations underline that sentinel behavior is probably a combination of an innate, imprinted pattern that is further affected by the experience. Future studies might further investigate this influence of experience, beyond innate behavior, on the group-specific sentinel behavior pattern in captive meerkats.

Acoustic structure and information content of trumpets in female Asian elephants (Elephas maximus).

Most studies on elephant vocal communication have focused on the low-frequency rumble, with less effort on other vocalization types such as the most characteristic elephant call, the trumpet. Yet, a better and more complete understanding of the elephant vocal system requires investigating other vocalization types and their functioning in more detail as well. We recorded adult female Asian elephants (Elephas maximus) at a private facility in Nepal and analyzed 206 trumpets from six individuals regarding their frequency, temporal and contour shape, and related acoustic parameters of the fundamental frequency. We also tested for information content regarding individuality and context. Finally, we recorded the occurrence of non-linear phenomena such as bifurcation, biphonation, subharmonics and deterministic chaos. We documented a mean fundamental frequency ± SD of 474 ± 70 Hz and a mean duration ± SD of 1.38 ± 1.46 s (Nindiv. = 6, Ncalls = 206). Our study reveals that the contour of the fundamental frequency of trumpets encodes information about individuality, but we found no evidence for trumpet subtypes in greeting versus disturbance contexts. Non-linear phenomena prevailed and varied in abundance among individuals, suggesting that irregularities in trumpets might enhance the potential for individual recognition. We propose that trumpets in adult female Asian elephants serve to convey an individual's identity as well as to signal arousal and excitement to conspecifics.

Operant control and call usage learning in African elephants.

Elephants exhibit remarkable vocal plasticity, and case studies reveal that individuals of African savannah (Loxodonta africana) and Asian (Elephas maximus) elephants are capable of vocal production learning. Surprisingly, however, little is known about contextual learning (usage and comprehension learning) in elephant communication. Usage learning can be demonstrated by training animals to vocalize in an arbitrary (cue-triggered) context. Here we show that adult African savannah elephants (n = 13) can vocalize in response to verbal cues, reliably producing social call types such as the low-frequency rumble, trumpets and snorts as well as atypical sounds using various mechanisms, thus displaying compound vocal control. We further show that rumbles emitted upon trainer cues differ significantly in structure from rumbles triggered by social contexts of the same individuals (n = 6). Every form of social learning increases the complexity of a communication system. In elephants, we only poorly understand their vocal learning abilities and the underlying cognitive mechanisms. Among other research, this calls for controlled learning experiments in which the prerequisite is operant/volitional control of vocalizations. This article is part of the theme issue 'Vocal learning in animals and humans'.

Vocal Creativity in Elephant Sound Production.

How do elephants achieve their enormous vocal flexibility when communicating, imitating or creating idiosyncratic sounds? The mechanisms that underpin this trait combine motoric abilities with vocal learning processes. We demonstrate the unusual production techniques used by five African savanna elephants to create idiosyncratic sounds, which they learn to produce on cue by positive reinforcement training. The elephants generate these sounds by applying nasal tissue vibration via an ingressive airflow at the trunk tip, or by contracting defined superficial muscles at the trunk base. While the production mechanisms of the individuals performing the same sound categories are similar, they do vary in fine-tuning, revealing that each individual has its own specific sound-producing strategy. This plasticity reflects the creative and cognitive abilities associated with 'vocal' learning processes. The fact that these sounds were reinforced and cue-stimulated suggests that social feedback and positive reinforcement can facilitate vocal creativity and vocal learning behavior in elephants. Revealing the mechanism and the capacity for vocal learning and sound creativity is fundamental to understanding the eloquence within the elephants' communication system. This also helps to understand the evolution of human language and of open-ended vocal systems, which build upon similar cognitive processes.

A novel theory of Asian elephant high-frequency squeak production.

BACKGROUND: Anatomical and cognitive adaptations to overcome morpho-mechanical limitations of laryngeal sound production, where body size and the related vocal apparatus dimensions determine the fundamental frequency, increase vocal diversity across taxa. Elephants flexibly use laryngeal and trunk-based vocalizations to form a repertoire ranging from infrasonic rumbles to higher-pitched trumpets. Moreover, they are among the few evolutionarily distantly related animals (humans, pinnipeds, cetaceans, birds) capable of imitating species-atypical sounds. Yet, their vocal plasticity has so far not been related to functions within their natural communicative system, in part because not all call types have been systematically studied. Here, we reveal how Asian elephants (Elephas maximus) produce species-specific squeaks (F0 300-2300 Hz) by using acoustic camera recordings to visualize sound emission and examining this alongside acoustic, behavioral, and morphological data across seven captive groups. RESULTS: We found that squeaks were emitted through the closed mouth in synchrony with cheek depression and retraction of the labial angles. The simultaneous emission of squeaks with nasal snorts (biphonation) in one individual confirmed that squeak production was independent of nasal passage involvement and this implicated oral sound production. The squeaks' spectral structure is incongruent with laryngeal sound production and aerodynamic whistles, pointing to tissue vibration as the sound source. Anatomical considerations suggest that the longitudinal closed lips function as the vibrators. Acoustic and temporal parameters exhibit high intra- and inter-individual variability that enables individual but no call-subtype classification. Only 19 of 56 study subjects were recorded to squeak, mostly during alarming contexts and social arousal but some also on command. CONCLUSION: Our results strongly suggest that Asian elephants force air from the small oral cavity through the tensed lips, inducing self-sustained lip vibration. Besides human brass players, lip buzzing is not described elsewhere in the animal kingdom. Given the complexity of the proposed mechanism, the surprising absence of squeaking in most of the unrelated subjects and the indication for volitional control, we hypothesize that squeak production involves social learning. Our study offers new insights into how vocal and cognitive flexibility enables mammals to overcome size-related limitations of laryngeal sound production. This flexibility enables Asian elephants to exploit a frequency range spanning seven octaves within their communicative system.

Airborne vocal communication in adult neotropical otters (Lontra longicaudis).

Most aquatic mammals have complex social and communication systems. Interestingly, little is known about otters' vocal communication compared to other aquatic mammals. Here, for the first time, we acoustically describe vocalizations of the neotropical otter (Lontra longicaudis), a solitary and endangered New World otter species. We recorded vocalizations and behavioral contexts from six captive neotropical otters at Projeto Lontra, Santa Catarina Island, Brazil. Analysis of acoustic parameters were used to classify the vocalizations according to structure and context. We describe six call types with highly tonal as well as chaotic vocalizations with fundamental frequencies ranging from 90 to 2500 Hz. Additionally, we identified sex differences in the usage of calls. Results suggest that the neotropical river otter has a rich vocal repertoire, similar in complexity to other solitary otter species, but less complex than that of the social giant otter. Despite differences in sociality, phylogeny and ecology, L. longicaudis seems to possess vocalizations homologous to those found in other otters (e.g. hah and chirp), suggesting phylogenetic inertia in otter communicative repertoire. Otters thus offer an interesting but neglected group to explore the evolution of communication systems.

Field Propagation Experiments of Male African Savanna Elephant Rumbles: A Focus on the Transmission of Formant Frequencies.

African savanna elephants live in dynamic fission⁻fusion societies and exhibit a sophisticated vocal communication system. Their most frequent call-type is the 'rumble', with a fundamental frequency (which refers to the lowest vocal fold vibration rate when producing a vocalization) near or in the infrasonic range. Rumbles are used in a wide variety of behavioral contexts, for short- and long-distance communication, and convey contextual and physical information. For example, maturity (age and size) is encoded in male rumbles by formant frequencies (the resonance frequencies of the vocal tract), having the most informative power. As sound propagates, however, its spectral and temporal structures degrade progressively. Our study used manipulated and resynthesized male social rumbles to simulate large and small individuals (based on different formant values) to quantify whether this phenotypic information efficiently transmits over long distances. To examine transmission efficiency and the potential influences of ecological factors, we broadcasted and re-recorded rumbles at distances of up to 1.5 km in two different habitats at the Addo Elephant National Park, South Africa. Our results show that rumbles were affected by spectral⁻temporal degradation over distance. Interestingly and unlike previous findings, the transmission of formants was better than that of the fundamental frequency. Our findings demonstrate the importance of formant frequencies for the efficiency of rumble propagation and the transmission of information content in a savanna elephant's natural habitat.

Corrigendum: Male African elephants discriminate and prefer vocalizations of unfamiliar females.

This corrects the article DOI: 10.1038/srep46414.

Sexual dimorphism in African elephant social rumbles.

This study used the source and filter theory approach to analyse sex differences in the acoustic features of African elephant (Loxodonta africana) low-frequency rumbles produced in social contexts ('social rumbles'). Permuted discriminant function analysis revealed that rumbles contain sufficient acoustic information to predict the sex of a vocalizing individual. Features primarily related to the vocalizer's size, i.e. fundamental frequency variables and vocal tract resonant frequencies, differed significantly between the sexes. Yet, controlling for age and size effects, our results indicate that the pronounced sexual size dimorphism in African elephants is partly, but not exclusively, responsible for sexual differences in social rumbles. This provides a scientific foundation for future work investigating the perceptual and functional relevance of specific acoustic characteristics in African elephant vocal sexual communication.

Male African elephants discriminate and prefer vocalizations of unfamiliar females.

Gaining information about conspecifics via long-distance vocalizations is crucial for social and spatially flexible species such as the African elephant (Loxodonta africana). Female elephants are known to discriminate individuals and kin based on acoustic cues. Specifically, females approached the loudspeaker exclusively with playbacks of familiar individuals with high association indexes, intentionally fusing with their affiliates. For males, which are less bonded, gathering social information via vocalizations could still have important implications, but little is known about their vocal discrimination skills. We experimentally tested the ability of male African elephants to discriminate the social rumbles of familiar (from the same population) versus unfamiliar females. Male elephants discriminated and preferentially moved towards the rumbles of unfamiliar females, showing longer attentive reactions and significantly more orientating (facing and approaching the speaker) behavior. The increased orientating response of males towards playbacks of unfamiliar females is converse to the reaction of female subjects. Our results provide evidence that male elephants extract social information from vocalizations, yet with a different intention than females. Accordingly, males might use social cues in vocalizations to assess mating opportunities, which may involve selection to identify individuals or kin in order to avoid inbreeding.

What Pinnipeds Have to Say about Human Speech, Music, and the Evolution of Rhythm.

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.

Information content and acoustic structure of male African elephant social rumbles.

Until recently, the prevailing theory about male African elephants (Loxodonta africana) was that, once adult and sexually mature, males are solitary and targeted only at finding estrous females. While this is true during the state of 'musth' (a condition characterized by aggressive behavior and elevated androgen levels), 'non-musth' males exhibit a social system seemingly based on companionship, dominance and established hierarchies. Research on elephant vocal communication has so far focused on females, and very little is known about the acoustic structure and the information content of male vocalizations. Using the source and filter theory approach, we analyzed social rumbles of 10 male African elephants. Our results reveal that male rumbles encode information about individuality and maturity (age and size), with formant frequencies and absolute fundamental frequency values having the most informative power. This first comprehensive study on male elephant vocalizations gives important indications on their potential functional relevance for male-male and male-female communication. Our results suggest that, similar to the highly social females, future research on male elephant vocal behavior will reveal a complex communication system in which social knowledge, companionship, hierarchy, reproductive competition and the need to communicate over long distances play key roles.

Establishing the fundamentals for an elephant early warning and monitoring system.

BACKGROUND: The decline of habitat for elephants due to expanding human activity is a serious conservation problem. This has continuously escalated the human-elephant conflict in Africa and Asia. Elephants make extensive use of powerful infrasonic calls (rumbles) that travel distances of up to several kilometers. This makes elephants well-suited for acoustic monitoring because it enables detecting elephants even if they are out of sight. In sight, their distinct visual appearance makes them a good candidate for visual monitoring. We provide an integrated overview of our interdisciplinary project that established the scientific fundamentals for a future early warning and monitoring system for humans who regularly experience serious conflict with elephants. We first draw the big picture of an early warning and monitoring system, then review the developed solutions for automatic acoustic and visual detection, discuss specific challenges and present open future work necessary to build a robust and reliable early warning and monitoring system that is able to operate in situ. FINDINGS: We present a method for the automated detection of elephant rumbles that is robust to the diverse noise sources present in situ. We evaluated the method on an extensive set of audio data recorded under natural field conditions. Results show that the proposed method outperforms existing approaches and accurately detects elephant rumbles. Our visual detection method shows that tracking elephants in wildlife videos (of different sizes and postures) is feasible and particularly robust at near distances. DISCUSSION: From our project results we draw a number of conclusions that are discussed and summarized. We clearly identified the most critical challenges and necessary improvements of the proposed detection methods and conclude that our findings have the potential to form the basis for a future automated early warning system for elephants. We discuss challenges that need to be solved and summarize open topics in the context of a future early warning and monitoring system. We conclude that a long-term evaluation of the presented methods in situ using real-time prototypes is the most important next step to transfer the developed methods into practical implementation.

Nocturnal "humming" vocalizations: adding a piece to the puzzle of giraffe vocal communication.

BACKGROUND: Recent research reveals that giraffes (Giraffa camelopardalis sp.) exhibit a socially structured, fission-fusion system. In other species possessing this kind of society, information exchange is important and vocal communication is usually well developed. But is this true for giraffes? Giraffes are known to produce sounds, but there is no evidence that they use vocalizations for communication. Reports on giraffe vocalizations are mainly anecdotal and the missing acoustic descriptions make it difficult to establish a call nomenclature. Despite inconclusive evidence to date, it is widely assumed that giraffes produce infrasonic vocalizations similar to elephants. In order to initiate a more detailed investigation of the vocal communication in giraffes, we collected data of captive individuals during day and night. We particularly focussed on detecting tonal, infrasonic or sustained vocalizations. FINDINGS: We collected over 947 h of audio material in three European zoos and quantified the spectral and temporal components of acoustic signals to obtain an accurate set of acoustic parameters. Besides the known burst, snorts and grunts, we detected harmonic, sustained and frequency-modulated "humming" vocalizations during night recordings. None of the recorded vocalizations were within the infrasonic range. CONCLUSIONS: These results show that giraffes do produce vocalizations, which, based on their acoustic structure, might have the potential to function as communicative signals to convey information about the physical and motivational attributes of the caller. The data further reveal that the assumption of infrasonic communication in giraffes needs to be considered with caution and requires further investigations in future studies.

Towards an Automated Acoustic Detection System for Free Ranging Elephants.

The human-elephant conflict is one of the most serious conservation problems in Asia and Africa today. The involuntary confrontation of humans and elephants claims the lives of many animals and humans every year. A promising approach to alleviate this conflict is the development of an acoustic early warning system. Such a system requires the robust automated detection of elephant vocalizations under unconstrained field conditions. Today, no system exists that fulfills these requirements. In this paper, we present a method for the automated detection of elephant vocalizations that is robust to the diverse noise sources present in the field. We evaluate the method on a dataset recorded under natural field conditions to simulate a real-world scenario. The proposed method outperformed existing approaches and robustly and accurately detected elephants. It thus can form the basis for a future automated early warning system for elephants. Furthermore, the method may be a useful tool for scientists in bioacoustics for the study of wildlife recordings.

Vocal learning in elephants: neural bases and adaptive context.

In the last decade clear evidence has accumulated that elephants are capable of vocal production learning. Examples of vocal imitation are documented in African (Loxodonta africana) and Asian (Elephas maximus) elephants, but little is known about the function of vocal learning within the natural communication systems of either species. We are also just starting to identify the neural basis of elephant vocalizations. The African elephant diencephalon and brainstem possess specializations related to aspects of neural information processing in the motor system (affecting the timing and learning of trunk movements) and the auditory and vocalization system. Comparative interdisciplinary (from behavioral to neuroanatomical) studies are strongly warranted to increase our understanding of both vocal learning and vocal behavior in elephants.

Age group estimation in free-ranging African elephants based on acoustic cues of low-frequency rumbles.

Animal vocal signals are increasingly used to monitor wildlife populations and to obtain estimates of species occurrence and abundance. In the future, acoustic monitoring should function not only to detect animals, but also to extract detailed information about populations by discriminating sexes, age groups, social or kin groups, and potentially individuals. Here we show that it is possible to estimate age groups of African elephants (Loxodonta africana) based on acoustic parameters extracted from rumbles recorded under field conditions in a National Park in South Africa. Statistical models reached up to 70 % correct classification to four age groups (infants, calves, juveniles, adults) and 95 % correct classification when categorising into two groups (infants/calves lumped into one group versus adults). The models revealed that parameters representing absolute frequency values have the most discriminative power. Comparable classification results were obtained by fully automated classification of rumbles by high-dimensional features that represent the entire spectral envelope, such as MFCC (75 % correct classification) and GFCC (74 % correct classification). The reported results and methods provide the scientific foundation for a future system that could potentially automatically estimate the demography of an acoustically monitored elephant group or population.