Visualizing Sound Emission of Elephant Vocalizations: Evidence for Two Rumble Production Types

Recent comparative data reveal that formant frequencies are cues to body size in animals, due to a close relationship between formant frequency spacing, vocal tract length and overall body size. Accordingly, intriguing morphological adaptations to elongate the vocal tract in order to lower formants occur in several species, with the size exaggeration hypothesis being proposed to justify most of these observations. While the elephant trunk is strongly implicated to account for the low formants of elephant rumbles, it is unknown whether elephants emit these vocalizations exclusively through the trunk, or whether the mouth is also involved in rumble production. In this study we used a sound visualization method (an acoustic camera) to record rumbles of five captive African elephants during spatial separation and subsequent bonding situations. Our results showed that the female elephants in our analysis produced two distinct types of rumble vocalizations based on vocal path differences: a nasally- and an orally-emitted rumble. Interestingly, nasal rumbles predominated during contact calling, whereas oral rumbles were mainly produced in bonding situations. In addition, nasal and oral rumbles varied considerably in their acoustic structure. In particular, the values of the first two formants reflected the estimated lengths of the vocal paths, corresponding to a vocal tract length of around 2 meters for nasal, and around 0.7 meters for oral rumbles. These results suggest that African elephants may be switching vocal paths to actively vary vocal tract length (with considerable variation in formants) according to context, and call for further research investigating the function of formant modulation in elephant vocalizations. Furthermore, by confirming the use of the elephant trunk in long distance rumble production, our findings provide an explanation for the extremely low formants in these calls, and may also indicate that formant lowering functions to increase call propagation distances in this species''.     

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ABSTRACT

Research on African elephant (Loxodonta africana) vocal communication has increased in recent years, yet there has been very little data collected on the vocal production of infant African elephants. Vocalizations were recorded from a group of five adult female African elephants and 3 dependent offspring (1 male and 2 female) at Disney's Animal Kingdom, Florida, U.S.A., using custom-designed audio-recording collars worn by the adult females. We measured both source and filter features of infant ‘rumble’ vocalizations made during affiliative social interactions and after cessation of nursing from adult females. Rumble vocalizations produced in the ‘nurse cessation’ context exhibited an upward shift in formant frequency locations, compared to rumbles produced during the ‘affiliation’ context. Additionally, call duration increased and fundamental frequencies decreased after nurse cessations for the male, but both females showed the opposite acoustic response. When infant rumbles accompanied nurse cessations, nursing was more likely to resume within 30 seconds compared to nurse cessations without vocalizations. These results suggest that infant rumbles associated with cessation of nursing reflect the motivational state of infants and may influence maternal responsiveness.     

A TECHNIQUE TO ‘TAG’ SPECIFIC VOCALIZATIONS IN TAPE-RECORDINGS OF COMPLEX VOCAL INTERACTIONS

ABSTRACT

It has been suggested that African savanna elephants Loxodonta africana produce 31 different call types (Langbauer 2000). Various researchers have described these calls by associating them with specific behavioural contexts. More recently Leong et al. (2003) have attempted to classify elephant call types based on their physical properties. They classified 8 acoustically distinct call types from a population of captive elephants. This study focuses on one of these call types, the rumble, in a wild population of elephants in Kruger National Park, South Africa. A single family group of elephants was followed to record group behaviours and vocalizations from January through August 2001. By measuring the physical properties of 663 rumbles and subjecting these to cluster analysis, we present evidence that shows that rumbles can be categorized by their physical properties and that the resulting rumble types are associated with specific group behaviours. We characterize three types of rumbles that differ significantly by ten acoustic parameters. Two rumble types were associated with the elephant group feeding and resting, while the third was associated with socializing and agitation.     

Wild Asian elephants distinguish aggressive tiger and leopard growls according to perceived danger

Prey species exhibit antipredator behaviours such as alertness, aggression and flight, among others, in response to predators. The nature of this response is variable, with animals reacting more strongly in situations of increased vulnerability. Our research described here is the first formal study to investigate night-time antipredator behaviour in any species of elephants, Asian or African. We examined the provocative effects of elephant-triggered tiger and leopard growls while elephants attempted to crop-raid. Tigers opportunistically prey on elephant calves, whereas leopards pose no threat; therefore, we predicted that the elephant response would be reflective of this difference. Elephants reacted similarly cautiously to the simulated presence of felids of both species by eventually moving away, but differed markedly in their more immediate behavioural responses. Elephants retreated silently to tiger-growl playbacks, whereas they responded with aggressive vocalizations, such as trumpets and grunts, to leopard-growl playbacks. Elephants also lingered in the area and displayed alert or investigative behaviours in response to leopard growls when compared with tiger growls. We anticipate that the methods outlined here will promote further study of elephant antipredator behaviour in a naturalistic context, with applications for conservation efforts as well.     

Perception of Vocal Tract Resonances by Whooping Cranes Grus americana

Although formants (vocal tract resonances) can often be observed in avian vocalizations, and several bird species have been shown to perceive formants in human speech sounds, no studies have examined formant perception in birds' own species-specific calls. We used playbacks of computer-synthesized crane calls in a modified habituation—dishabituation paradigm to test for formant perception in whooping cranes ( Grus americana ). After habituating birds to recordings of natural contact calls, we played a synthesized replica of one of the habituating stimuli as a control to ensure that the synthesizer worked adequately; birds dishabituated in only one of 13 cases. Then, we played the same call with its formant frequencies shifted. The birds dishabituated to the formant-shifted calls in 10 out of 12 playbacks. These data suggest that cranes perceive and attend to changes in formant frequencies in their own species-specific vocalizations, and are consistent with the hypothesis that formants can provide acoustic cues to individuality and body size.     

The stomatopod rumble: Low frequency sound production in Hemisquilla californiensis

Stomatopods (mantis shrimp), numbering over 450 species, are renowned for their exceptional visual and chemosensory abilities and yet virtually nothing is known about their use of acoustic signals. We present acoustic recordings and analyses of the sounds of a stomatopod, Hemisquilla californiensis. This species generates tonal, low frequency sounds, which we term 'rumble', that are spectrally similar to those produced by African and Asian elephants. The fundamental frequency of the stomatopod rumble ranges from 20 to 60 Hz, with a strong second harmonic. Hemisquilla californiensis appears to generate these sounds through contractions of the posterior mandibular remotor muscle which is coupled to a stiff, lateral extension of the carapace. The sides of the carapace are covered by large, polarized, red spots which vibrate during sound production. Thus, the animals may generate a multi-modal signal by coupling vibrational and visual signals. Hemisquilla californiensis generates the rumble while interacting with potential predators and burrow intruders, suggesting a defensive or territorial function for the sound.     

Age Differences in the Responses to Adult and Juvenile Alarm Calls by Bonnet Macaques (Macaca radiata)

This study examined the differential responses to alarm calls from juvenile and adult wild bonnet macaques ( Macaca radiata ) in two parks in southern India. Field studies of several mammalian species have reported that the alarm vocalizations of immature individuals are often treated by perceivers as less provocative than those of adults. This study documents such differences in response using field-recorded playbacks of juvenile and adult alarm vocalizations. To validate the use of playback vocalizations as proxies of natural calls, we compared the responses of bonnet macaques to playbacks of alarm vocalizations with responses engendered by natural alarm vocalizations. We found that the frequency of flight, latency to flee, and the frequency of scanning to vocalization playbacks and natural vocalizations were comparable, thus supporting the use of playbacks to compare the effects of adult and juvenile calls. Our results showed that adult alarm calls were more provocative than juvenile alarm calls, inducing greater frequencies of flight with faster reaction times. Conversely, juvenile alarm calls were more likely to engender scanning by adults, a result interpreted as reflecting the lack of reliability of juvenile calls. Finally, we found age differences in flight behavior to juvenile alarm calls and to playbacks of motorcycle engine sounds, with juveniles and subadults more likely to flee than adults after hearing such sounds. These findings might reflect an increased vulnerability to predators or a lack of experience in young bonnet macaques.     

Pilot Whales Attracted to Killer Whale Sounds: Acoustically-Mediated Interspecific Interactions in Cetaceans

In cetaceans’ communities, interactions between individuals of different species are often observed in the wild. Yet, due to methodological and technical challenges very little is known about the mediation of these interactions and their effect on cetaceans’ behavior. Killer whales (Orcinus orca) are a highly vocal species and can be both food competitors and potential predators of many other cetaceans. Thus, the interception of their vocalizations by unintended cetacean receivers may be particularly important in mediating interspecific interactions. To address this hypothesis, we conducted playbacks of killer whale vocalizations recorded during herring-feeding activity to free-ranging long-finned pilot whales (Globicephala melas). Using a multi-sensor tag, we were able to track the whales and to monitor changes of their movements and social behavior in response to the playbacks. We demonstrated that the playback of killer whale sounds to pilot whales induced a clear increase in group size and a strong attraction of the animals towards the sound source. These findings provide the first experimental evidence that the interception of heterospecific vocalizations can mediate interactions between different cetacean species in previously unrecognized ways.     

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.     

Little Evidence to Support the Risk–Disturbance Hypothesis as an Explanation for Responses to Anthropogenic Noise by Pygmy Marmosets (Cebuella niveiventris) at a Tourism site in the Peruvian Amazon

The risk–disturbance hypothesis states that animals react to human stressors in the same way as they do to natural predators. Given increasing human–wildlife contact, understanding whether animals perceive anthropogenic sounds as a threat is important for assessing the long-term sustainability of wildlife tourism and proposing appropriate mitigation strategies. A study of pygmy marmoset (Cebuella niveiventris) responses to human speech found marmosets fled, decreased feeding and resting, and increased alert behaviors in response to human speech. Following this study, we investigated pygmy marmoset reactions to playbacks of different acoustic stimuli: controls (no playback, white noise and cicadas), anthropogenic noise (human speech and motorboats), and avian predators. For each playback condition, we recorded the behavior of a marmoset and looked at how the behaviors changed during and after the playback relative to behaviors before. We repeated this on ten different marmoset groups, playing each condition once to each group. The results did not replicate a previous study on the same species, at the same site, demonstrating the importance of replication in primate research, particularly when results are used to inform conservation policy. The results showed increased scanning during playbacks of the cicadas and predators compared with before the playback, and an increase in resting after playbacks of avian predators, but no evidence of behavior change in response to playbacks of human speech. There was no effect of ambient sound levels or distance between the playback source and focal animals on their behavior for all playback conditions. Although we find that noise can change the behavior of pygmy marmosets, we did not find evidence to support the risk–disturbance hypothesis.

     

Admixture in Africanized honey bees (Apis mellifera) from Panamá to San Diego,California (U.S.A.)

The Africanized honey bee (AHB) is a New World amalgamation of several subspecies of the western honey bee (Apis mellifera), a diverse taxon historically grouped into four major biogeographic lineages: A (African), M (Western European), C (Eastern European), and O (Middle Eastern). In 1956, accidental release of experimentally bred “Africanized” hybrids from a research apiary in Sao Paulo, Brazil initiated a hybrid species expansion that now extends from northern Argentina to northern California (U.S.A.). Here, we assess nuclear admixture and mitochondrial ancestry in 60 bees from four countries (Panamá; Costa Rica, Mexico; U.S.A) across this expansive range to assess ancestry of AHB several decades following initial introduction and test the prediction that African ancestry decreases with increasing latitude. We find that AHB nuclear genomes from Central America and Mexico have predominately African genomes (76%–89%) with smaller contributions from Western and Eastern European lineages. Similarly, nearly all honey bees from Central America and Mexico possess mitochondrial ancestry from the African lineage with few individuals having European mitochondria. In contrast, AHB from San Diego (CA) shows markedly lower African ancestry (38%) with substantial genomic contributions from all four major honey bee lineages and mitochondrial ancestry from all four clades as well. Genetic diversity measures from all New World populations equal or exceed those of ancestral populations. Interestingly, the feral honey bee population of San Diego emerges as a reservoir of diverse admixture and high genetic diversity, making it a potentially rich source of genetic material for honey bee breeding.     

Non‐Selective and Time‐Dependent Behavioural Responses of Common Toads (Bufo bufo) to Predator Acoustic Cues

Acoustic predator recognition has rarely been studied in anurans, in spite of the fact that hearing is widespread in these animals and that it has been demonstrated to play an important role in both arthropods and other vertebrates. Using field playback experiments, we tested the hypothesis that adult common toads (Bufo bufo) are capable of recognizing natural vocalizations of a common predator, the Eurasian otter (Lutra lutra), and show antipredator responses. We found that toads exposed to both natural (two types of otter sounds) and synthetic stimuli [white noise (WN) and otter sound‐based amplitude modulated WN] increased time allocated to locomotion and escape behaviour. These responses were correlated with time elapsed from sunset to the onset of testing and were independent from the type of acoustic signal, toad features and other environmental factors monitored. We conclude that B. bufo has not developed a selective recognition of predator vocalizations, suggesting that low‐frequency or seismic sounds associated with predator movements may provide anurans with better cues about an approaching risk. We propose that the time‐dependent response to acoustic stimuli of common toads represents a case of threat‐sensitivity and demonstrates that it can occur even when the response to the threat is not predator specific.     

Acoustically mediated individual recognition by a coral reef fish (Pomacentrus partitus)

Acoustically mediated individual recognition has been demonstrated in the field by males of the bicolor damselfish Pomacentrus partitus Poey. Playbacks of non-resident sounds from a given fish's territory elicited a greater response from its nearest neighbour than playbacks of the resident's sound—in accordance with the predictions of the ‘dear-enemy’ effect. Testing also included switching the sounds of the two nearest neighbours relative to each respective male's territory. Results demonstrated that all males in the colony individually recognized the sounds of their two nearest neighbours.     

Invasion of the acoustic niche: variable responses by native species to invasive American bullfrog calls

Biological invasions are a major threat to biodiversity. Invasive species that use acoustic communication can affect native species through interference in the acoustic niche. The American Bullfrog Lithobates catesbeianus is a highly invasive anuran that is widely distributed in the Brazilian Atlantic Rainforest. Adult male bullfrogs emit loud advertisement calls at frequencies that overlap with the calls of several native species of frogs. Given that spectral overlap is a major factor in acoustic masking, the purpose of this study was to test the effects of the acoustic invasion of L. catesbeianus on native frogs that have calls with and without spectral overlap with the invader. In field experiments, we exposed calling males of two overlapping species and two non-overlapping species to recorded bullfrog vocalizations, white noise, and the vocalization of another native frog species. To identify effects, we compared calls recorded before, during, and after exposure. Our results showed that native species altered their calls in response to the bullfrog calls. However, we also observed similar responses to white noise and heterospecific native calls. Both the invasive and heterospecific calls were emitted at low frequencies, which suggests that the observed responses might be specific to low-frequency calls. Our results provide evidence that the introduction of new sounds can cause native species to modify their calls, and that responses to exogenous sounds are species- and stimulus-specific.     

Responses of Redfronted Lemurs to Experimentally Modified Alarm Calls: Evidence for Urgency-Based Changes in Call Structure

Abstract The aim of this study was to investigate how information about the affective state is expressed in vocalizations. Alarm calls can serve as model systems with which to study this general question. Therefore, we examined the information content of terrestrial predator alarm calls of redfronted lemurs ( Eulemur fulvus rufus ), group-living Malagasy primates. Redfronted lemurs give specific alarm calls only towards raptors, whereas calls given in response to terrestrial predators (woofs) are also used in other situations characterized by high arousal. Woofs may therefore have the potential to express the perceived risk of a given threat. In order to examine whether different levels of arousal are expressed in call structure, we analysed woofs given during inter-group encounters or in response to playbacks of a barking dog, assuming that animals engaged in inter-group encounters experience higher arousal than during the playbacks of dog barks. A multivariate acoustic analysis revealed that calls given during group encounters were characterized by higher frequencies than calls given in response to playbacks of dog barks. In order to examine whether this change in call structure is salient to conspecifics, we conducted playback experiments with woofs, modified in either amplitude or frequencies. Playbacks of calls with increased frequency or amplitude elicited a longer orienting response, suggesting that different levels of arousal are expressed in call structure and provide meaningful information for listeners. In conclusion, the results of our study indicate that the information about the sender's affective state is expressed in the structure of vocalizations.     

Elephant calling patterns as indicators of group size and composition: the basis for an acoustic monitoring system

The paper gives evidence that the vocal activity of elephants varies with group size, composition and reproductive status, and that elephants' calling patterns could therefore provide the basis for a remote monitoring system. We examined a 3‐week set of array‐based audio recordings of savanna elephants (Loxodonta africana), searching for diagnostic acoustic parameters. An acoustic array made it possible to locate recorded sounds and attribute the calls to particular elephants or elephant groups. Simultaneous video recordings made it possible to document visible behaviour and roughly correlate it with vocalizations. We compared several measures of call density in elephant groups containing up to 59 individuals, and found that rates of calling increased with increasing numbers of elephants. We divided all call events into three structural types (single‐voice low‐frequency calls, multiple‐voice clustered low‐frequency calls, and single‐voice high frequency calls), and found that the incidence of these varies predictably with group composition. These results suggest the value of a network of listening systems in remote areas for the collection of information on elephant abundance and population structure.     

Model vs. playback experiments: The impact of sensory mode on predator-specific escape responses in saki monkeys

Although experimentally simulating predator presence helps improve sample sizes in studies of free-ranging animals, few studies have examined whether auditory playbacks and visual models produce similar results. Additionally, it is unclear if anti-predator strategies are specific to predator hunting styles in understudied Neotropical pitheciid primates, limiting what we can generalize about this phenomenon across this taxonomic order. We conducted predator simulation experiments to assess whether wild Rylands' bald-faced saki monkeys (Pithecia rylandsi) recognize predators based solely on acoustic cues, exhibit predator-specific responses to different predator types, and vary responses to presentations in different sensory modes. In our playback experiments, sakis had weak responses to non-predator control vocalizations compared to jaguar growls and harpy eagle shrieks. In most predator playbacks, subjects' first glance corresponded to the direction from which simulated predators would typically attack (above vs. below). However, although sakis exhibited appropriate movement responses to harpy playbacks (i.e., descending canopy), they exhibited no clear movement patterns when presented with jaguar playbacks. In contrast, jaguar model experiments consistently elicited fast approaches, mobbing-style responses, and long alarm calling bouts. Thus, if we had relied on playbacks alone, we might have concluded that sakis have only generalized responses to terrestrial ambush predators. In fact, in all variables measured (e.g., latency, number of calls, and response duration), models of both predator species elicited stronger reactions than playbacks. Results indicate that bald-faced sakis can identify predators based solely on vocalizations, but do not exhibit predator-specific escape responses to terrestrial predators based on acoustic cues alone. The differential response to playbacks and models calls into question the reliability of using acoustic-only stimuli to assess the specificity of anti-predator behavior to predator hunting styles in some primate species.     

Noise-Induced Frequency Modifications of Tamarin Vocalizations: Implications for Noise Compensation in Nonhuman Primates

Previous research suggests that nonhuman primates have limited flexibility in the frequency content of their vocalizations, particularly when compared to human speech. Consistent with this notion, several nonhuman primate species have demonstrated noise-induced changes in call amplitude and duration, with no evidence of changes to spectral content. This experiment used broad- and narrow-band noise playbacks to investigate the vocal control of two call types produced by cotton-top tamarins (Saguinus Oedipus). In ‘combination long calls’ (CLCs), peak fundamental frequency and the distribution of energy between low and high frequency harmonics (spectral tilt) changed in response to increased noise amplitude and bandwidth. In chirps, peak and maximum components of the fundamental frequency increased with increasing noise level, with no changes to spectral tilt. Other modifications included the Lombard effect and increases in chirp duration. These results provide the first evidence for noise-induced frequency changes in nonhuman primate vocalizations and suggest that future investigations of vocal plasticity in primates should include spectral parameters.     

Alarm Calls of Marmosets (Callithrix geoffroyi) to Snakes and Perched Raptors

Communication about the presence of predators is an important benefit of group living. Critical information about the nature of danger can be conveyed through referential alarm calls. Raptors pose a significant predatory threat to callitrichid species. Unlike a raptor in flight, a perched raptor cannot attack suddenly at great speed, and it can be monitored from a safe distance. In this sense a perched bird may pose a threat more similar to that of a terrestrial predator such as a snake. Here we compare predatory contexts by addressing these two questions: 1) Do marmosets produce acoustically distinct alarm calls to snake models and perched raptor models? 2) Do the visual responses of the marmosets to the playbacks of perched raptor–elicited calls differ from those given to the playbacks of calls given in response to snakes? We recorded alarm calls from two groups of outdoor-housed Geoffroy’s marmosets (Callithrix geoffroyi) in response to predator models. Later, we played back stimuli created from these recordings to the marmosets and scored their gaze direction. Results show that calls given to models of perched raptors are acoustically distinct from those given to models of snakes. Further, the relative number of upward to downward looks while listening to the playbacks of perched raptor–elicited calls was significantly greater than it was for snake-elicited calls. Reactions to airborne raptors are known to elicit freezing or rapid flight, neither of which occurred in response to our playbacks. Our data suggest a greater complexity in the alarm call repertoire of marmosets than previously demonstrated.     

Metabolic response to alarm pheromone in honey bees

Exposure to alarm pheromone elicits increases in oxidative metabolism in Apis mellifera. The following quantitative results are reported: (1) The alarm response, measured by short-term elevated oxygen consumption in each bee, increases with increasing numbers of bees in the test groups. The rate of increase in response per bee shows a group effect which is greatest in small groups (1–100 bees) and remains constant in larger groups (up to 6,700 bees). (2) The pheromone concentration affects the reaction elicited. The greater the dose, the larger is the reaction up to a concentration of 2.4 μg/ml. Greater doses elicit no greater response. (3) Response to the pheromone by winter bees is maximum at 20°C and decreases at air temperatures above or below this value. (4) This metabolic reaction may provide a tool for quantitating temperament of honey bees.