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Many vertebrates eavesdrop on alarm calls of other species, as well as responding to their own species' calls, but eavesdropping on heterospecific alarm calls might be harder than conspecific reception when environmental conditions make perception or recognition of calls difficult. This could occur because individuals lack hearing specializations for heterospecific calls, have less familiarity with them, or require more details of call structure to identify calls they have learned to recognize. We used a field playback experiment to provide a direct test of whether noise, as an environmental perceptual challenge, reduces response to heterospecific compared to conspecific alarm calls. We broadcast superb fairy-wren (Malurus cyaneus) and white-browed scrubwren (Sericornis frontalis) flee alarm calls to each species with or without simultaneous broadcast of ambient noise. Using two species allows isolation of the challenge of heterospecific eavesdropping independently of any effect of call structure on acoustic masking. As predicted, birds were less likely to flee to heterospecific than conspecific alarm calls during noise. We conclude that eavesdropping was harder in noise, which means that noise could disrupt information on danger in natural eavesdropping webs and so compromise survival. This is particularly significant in a world with increasing anthropogenic noise.
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Passeriformes , Aves Canoras , Humanos , Animais , Vocalização Animal/fisiologia , Ruído , Aves Canoras/fisiologia , Passeriformes/fisiologia , AprendizagemRESUMO
The alarm calls of vervet monkeys (Chlorocebus pygerythrus) have been the subject of considerable focus by researchers, owing primarily to the purported referential qualities of different alarm call types. With this focus on reference, acoustic variation among calls elicited by the same range of predators has typically been overlooked. Specifically, at least one type of alarm call-the terrestrial alarm-was described over 50 years ago as being acoustically distinct between males and females-a description that has largely eluded more systematic scrutiny. Here, we provide a quantitative acoustic analysis and comparison of terrestrial alarm calls produced by adult male and female vervet monkeys. We use a random forest model to determine which acoustic variables best distinguish between the calls of males and females, and use an unsupervised clustering technique to objectively determine whether alarms produced by each sex fall into discrete types. We found that the calls of males and females differed most in frequency-based parameters, with male alarms containing more energy at lower frequencies relative to females. Calls produced by males were also of longer duration, and consisted of longer individual call elements relative to female calls. While calls generally fell into clusters associated with either male or female alarms, we found that some fell into atypical clusters given the caller's sex, and that the clusters themselves showed evidence of intergradation. We discuss these results in terms of potential differences in the function of, and motivation for, calling by males and females. We emphasize the need for a more holistic approach to the classification of vocal signals that considers contextual, functional, and structural variation.
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Primate alarm calls are mainly hardwired but individuals need to adapt their calling behaviours according to the situation. Such learning necessitates recognising locally relevant dangers and may take place via their own experience or by observing others. To investigate monkeys alarm calling behaviour, we carried out a field experiment in which we exposed juvenile vervet monkeys to unfamiliar raptor models in the presence of audiences that differed in experience and reliability. We used audience age as a proxy for experience and relatedness as a proxy for reliability, while quantifying audience reactions to the models. We found a negative correlation between alarm call production and callers' age. Adults never alarm called, compared to juveniles. We found no overall effect of audience composition and size, with juveniles calling more when with siblings than mothers or unrelated individuals. Finally, concerning audience reactions to the models, we observed juveniles remained silent with vigilant mothers and only alarm called with ignoring mothers, whereas we observed the opposite for siblings: juveniles remained silent with ignoring siblings and called with vigilant siblings. Despite the small sample size, juvenile vervet monkeys, confronted with unfamiliar and potentially dangerous raptors, seem to rely on others to decide whether to alarm call, demonstrating that the choice of the model may play an important key role in the ontogeny of primate alarm call behaviour.
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Primatas , Vocalização Animal , Feminino , Chlorocebus aethiops , Animais , Humanos , Reprodutibilidade dos Testes , Haplorrinos , MãesRESUMO
Alarm signals have evolved to communicate pertinent threats to conspecifics, but heterospecifics may also use alarm calls to obtain social information. In birds, mixed-species flocks are often structured around focal sentinel species, which produce reliable alarm calls that inform eavesdropping heterospecifics about predation risk. Prior research has shown that Neotropical species innately recognize the alarm calls of a Nearctic sentinel species, but it remains unclear how generalizable or consistent such innate signal recognition of alarm-calling species is. We tested for the responses to the alarm calls of a Neotropical sentinel forest bird species, the dusky-throated antshrike (Thamnomanes ardesiacus), by naive resident temperate forest birds across three continents during the winter season. At all three sites, we found that approaches to the Neotropical antshrike alarm calls were similarly frequent to the alarm calls of a local parid sentinel species (positive control), while approaches to the antshrike's songs and to non-threatening columbid calls (negative controls) occurred significantly less often. Although we only tested one sentinel species, our findings indicate that temperate forest birds can recognize and adaptively respond globally to a foreign and unfamiliar tropical alarm call, and suggest that some avian alarm calls transcend phylogenetic histories and individual ecological experiences.
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Passeriformes , Vocalização Animal , Animais , Vocalização Animal/fisiologia , Filogenia , Florestas , Passeriformes/fisiologia , Comportamento PredatórioRESUMO
BACKGROUND: Predator avoidance can have immense impacts on fitness, yet individual variation in the expression of anti-predator behaviour remains largely unexplained. Existing research investigating learning of novel predators has focused either on individuals or groups, but not both. Testing in individual settings allows evaluations of learning or personality differences, while testing in group settings makes it impossible to distinguish any such individual differences from social dynamics. In this study, we investigate the effect of social dynamics on individual anti-predator behaviour. We trained 15 captive ravens to recognize and respond to a novel experimental predator and then exposed them to this predator in both group and isolation settings across 1.5 years to tease apart individual differences from social effects and evaluate two hypotheses: (1) weaker anti-predator responses of some individuals in the group occurred, because they failed to recognize the experimental predator as a threat, leading to weak responses when separated, or (2) some individuals had learned the new threat, but their scolding intensity was repressed in the group trials due to social dynamics (such as dominance rank), leading to increased scolding intensity when alone. RESULTS: We found that dominance significantly influences scolding behaviour in the group trials; top-ranked individuals scold more and earlier than lower ranking ones. However, in the separation trials scolding duration is no longer affected by rank. CONCLUSIONS: We speculate that, while top-ranked individuals use their anti-predator responses to signal status in the group, lower-ranking ravens may be suppressed from, or are less capable of, performing intense anti-predator behaviour while in the group. This suggests that, in addition to its recruitment or predator-deterrent effects, alarm calling may serve as a marker of individual quality to conspecifics.
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Red-backed shrikes (Lanius collurio) show a substantial variability in their nest defence behaviour, which usually follows the rules of optimal parental behaviour, vigorously attacking egg and chick predators and only passively guarding against harmless animals. Nevertheless, shrikes hesitate to attack the Eurasian magpie (Pica pica), which specializes in plundering passerine nests. Our previous studies have suggested that this behaviour may be the result of an alternative defence strategy, relying on nest crypsis. To test this hypothesis, at the shrike nests, we presented a magpie dummy associated with playbacks drawing the predators' attention to the presence of the nest. We predicted that the presentation of a magpie dummy associated with shrike alarm calls moves the parents to action, causing them to chase the magpie away from the nest. We showed that the presence of a magpie dummy associated with shrike alarm calls elicits a significantly more active response in shrike parents compared to a magpie dummy associated with neutral song. Parents actively moved around the dummy and produced alarm calls; nevertheless, most of the tested pairs hesitated to attack the dummy. We may conclude that the low nest defence activity of shrike parents towards magpie dummy was partly the result of an alternative strategy, which may be cancelled out by alerting the predator to the location of the nest; nevertheless, shrikes seem to be afraid of the magpie and hesitate to attack it physically.
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Passeriformes , Comportamento Predatório , Animais , Masculino , Passeriformes/fisiologia , Comportamento Predatório/fisiologiaRESUMO
Animal biologists have recently focused on individual variation in behavioral traits and have found that individuals of many species have personalities. These are defined as consistent intraspecific differences in behaviors that are repeatable across different situations and stable over time. When animals sense danger, some individuals will alert neighbors with alarm calls and both calling and responding vary consistently among individuals. Plants, including sagebrush, emit volatile cues when they are attacked by herbivores and neighbors perceive these cues and reduce their own damage. We experimentally transferred volatiles between pairs of sagebrush plants to evaluate whether individuals showed consistent variation in their effectiveness as emitters and as receivers of cues, measured in terms of reduced herbivore damage. We found that 64% of the variance in chewing damage to branches over the growing season was attributable to the identity of the individual receiving the cues. This variation could have been caused by inherent differences in the plants as well as by differences in the environments where they grew and their histories. We found that 5% of the variance in chewing damage was attributable to the identity of the emitter that provided the cue. This fraction of variation was statistically significant and could not be attributed to the environmental conditions of the receiver. Effective receivers were also relatively effective emitters, indicating consistency across different situations. Pairs of receivers and emitters that were effective communicators in 2018 were again relatively effective in 2019, indicating consistency over time. These results suggest that plants have repeatable individual personalities with respect to alarm calls.
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Artemisia , Compostos Orgânicos Voláteis , Animais , Herbivoria , Personalidade , PlantasRESUMO
BACKGROUND: The rutting vocal display of male impala Aepyceros melampus is unique for its complexity among ruminants. This study investigates bouts of rutting calls produced towards potential mates and rival males by free-ranging male impala in Namibia. In particular, a comparison of male rutting and alarm snorts is conducted, inspired by earlier findings of mate guarding by using alarm snorts in male topi Damaliscus lunatus. RESULTS: Rutting male impala produced 4-38 (13.5 ± 6.5) rutting calls per bout. We analyzed 201 bouts, containing in total 2709 rutting calls of five types: continuous roars produced within a single exhalation-inhalation cycle; interrupted roars including few exhalation-inhalation cycles; pant-roars distinctive by a pant-phase with rapidly alternating inhalations and exhalations; usual snorts lacking any roar part; and roar-snorts starting with a short roar part. Bouts mostly started and ended with usual snorts. Continuous roars were the shortest roars. The average duration of the exhalatory phase was longest in the continuous roars and shortest in the pant-roars. The average fundamental frequency (49.7-51.4 Hz) did not differ between roar types. Vocal tract length, calculated by using measurements of the first four vocal tract resonances (formants), ranged within 381-382 mm in all roar types. In the studied male impala, rutting snorts within bouts of rutting calls were longer and had higher values of the upper quartile in the call spectra than alarm snorts produced towards potential danger. CONCLUSIONS: Additional inhalations during the emission of the interrupted and pant-roars prolong their duration compared to the continuous roars but do not affect the fundamental frequency or the degree of larynx retraction while roaring. Alarm snorts are separated from one another by large intervals, whereas the intervals between rutting snorts within bouts are short. Sometimes, rutting snorts alternate with roars, whereas alarm snorts do not. Therefore, it is not the acoustic structure of individual snorts but the temporal sequence and the occasional association with another call type that defines snorts as either rutting or alarm snorts. The rutting snorts of male impala may function to attract the attention of receptive females and delay their departure from a male's harem or territory.
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The ability to use heterospecific alarm calls is adaptive in the wild, as it provides an opportunity to avoid predators. We now know that several species are able to respond to alarm calls intended for others. However, this capacity has never been investigated in domestic animals. The capacity to use heterospecific alarm calls may be relevant for free-range domestic species, especially when they share predators with wild signallers. Using playback experiments, we investigated the vigilance behaviour of free-range naked neck chickens (Gallus gallus domesticus) when confronted with alarm calls (test playbacks) and songs (control playbacks) of a commonly occurring wild passerine, the great tit (Parus major). We found that subjects exhibited an increased vigilance to alarm calls compared to songs, therefore, showing that chickens respond to heterospecific signals as wild birds do. Recently, there has been an increased interest for free-range poultry production, notably because of the benefits of this farming method for chicken welfare. Although future studies are required to address this question, mortality due to predation may be reduced through the implementation of structures in areas frequented by wild heterospecific signallers.
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Galinhas , Passeriformes , Animais , Comportamento Predatório , Vocalização AnimalRESUMO
In the perpetual struggle between high-speed predators and their prey, individuals need to react in the blink of an eye to avoid capture. Alarm calls that warn of danger therefore need to do so sufficiently rapidly that listeners can escape in time. Paradoxically, many species produce more elements in their alarm calls when signalling about more immediate danger, thereby increasing the reliability of transmission of critical information but taking longer to convey the urgent message. We found that New Holland honeyeaters, Phylidonyris novaehollandiae, incorporated more elements in alarm calls given to more dangerous predators, but video analysis revealed that listeners responded in 100 ms, after only the first element. Consistent with this rapid response, the acoustic structure of the first element varied according to the danger, and playbacks confirmed that birds need hear only the first element to assess risk. However, birds hid for longer and were more likely to flee, after calls with more elements. The dual mechanisms of varying both element structure and number may provide a widespread solution to signalling rapidly and reliably about immediate danger.
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Aves Canoras/fisiologia , Vocalização Animal/fisiologia , Animais , Reação de Fuga/fisiologia , PasseriformesRESUMO
Communication plays a vital role in the social lives of many species and varies greatly in complexity. One possible way to increase communicative complexity is by combining signals into longer sequences, which has been proposed as a mechanism allowing species with a limited repertoire to increase their communicative output. In mammals, most studies on combinatoriality have focused on vocal communication in non-human primates. Here, we investigated a potential combination of alarm calls in the dwarf mongoose (Helogale parvula), a non-primate mammal. Acoustic analyses and playback experiments with a wild population suggest: (i) that dwarf mongooses produce a complex call type (T3) which, at least at the surface level, seems to comprise units that are not functionally different to two meaningful alarm calls (aerial and terrestrial); and (ii) that this T3 call functions as a general alarm, produced in response to a wide range of threats. Using a novel approach, we further explored multiple interpretations of the T3 call based on the information content of the apparent comprising calls and how they are combined. We also considered an alternative, non-combinatorial interpretation that frames T3 as the origin, rather than the product, of the individual alarm calls. This study complements previous knowledge of vocal combinatoriality in non-primate mammals and introduces an approach that could facilitate comparisons between different animal and human communication systems.
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Herpestidae , Vocalização Animal , Animais , Comportamento SocialRESUMO
Several theories have been generated to understand the socio-cognitive mechanisms underlying the unique cooperative abilities of humans. The 'interdependence hypothesis' posits first, that the cognitive dimension of human cooperation evolved in contexts when several individuals needed to act together to achieve a common goal, like when hunting large prey. Second, the more interdependent individuals are, the more likely they are to provide services to conspecifics in other contexts. Alternatively, the 'social tolerance hypothesis' proposes that higher social tolerance allows conspecifics to cooperate more efficiently and with a wider range of partners. We conducted the first field experimental evaluation of both hypotheses in our closest living relatives by contrasting chimpanzees to the less interdependent but more tolerant bonobos. We compared each species' performance during a cooperative task: informing conspecifics about a danger. We presented Gaboon viper models to 82 individuals from five wild communities. Chimpanzees arriving late at the snake were significantly more likely to have heard a call and less likely to startle, indicating that chimpanzees were better informed about the presence of the threat than bonobos. This stems from clear species differences in how individuals adjusted their calling decisions to the level of information already available. Chimpanzees were more likely to call and produced more alarm calls when they had not yet heard a call, whereas bonobos did so when they already heard a call. Our results confirm the link between interdependence and cooperation performance. These species differences were most likely driven by differences in motivation rather than in cognitive capacities because both species tended to consider audience knowledge in their decision to call. Our results inform theories on the evolution of human cooperation by linking inter-group competition pressure and in-group cooperative motivation and/or capability.
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Comportamento Animal , Pan paniscus/fisiologia , Pan troglodytes/fisiologia , Comportamento Social , Animais , Cognição , Comportamento Cooperativo , SerpentesRESUMO
Information about predation risk is of fundamental value in biological communities. Because many prey species have shared predators, eavesdropping on other species' alarms is a widely recognized mechanism underlying the formation of mixed-species groups. However, information transfer may vary both across and within groups because some species provide higher-quality information about predators than others. We tested this phenomenon in Amazonian understory mixed-species flocks of birds in which two sentinel species-the bluish-slate antshrike (Thamnomanes schistogynus) and the dusky-throated antshrike (Thamnomanes ardesiacus)-occupy different habitats and provide alarm calls that are used by eavesdropping flock mates. In a playback experiment, two associate species responded significantly more strongly to alarm calls from the same sentinel species, reflecting the greater reliability of information about predator threats that could affect survival and habitat choice. Our work provides evidence of a repeated asymmetry across space in the available information about threats.
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Comportamento Animal , Passeriformes/fisiologia , Vocalização Animal , Animais , Ecossistema , Peru , Comportamento Predatório , Floresta Úmida , Especificidade da EspécieRESUMO
Information about predators can mean the difference between life and death, but prey face the challenge of integrating personal information about predators with social information from the alarm calls of others. This challenge might even affect the structure of interspecific information networks: species vary in response to alarm calls, potentially because different foraging ecologies constrain the acquisition of personal information. However, the hypothesis that constrained personal information explains a greater response to alarm calls has not been experimentally tested. We used a within-species test to compare the antipredator responses of New Holland honeyeaters, Phylidonyris novaehollandiae, during contrasting foraging behaviour. Compared with perched birds, which hawk for insects and have a broad view, those foraging on flowers were slower to spot gliding model predators, showing that foraging behaviour can affect predator detection. Furthermore, nectar-foraging birds were more likely to flee to alarm call playbacks. Birds also assessed social information relevance: more distant calls, and those from another species, prompted fewer flights and slower reaction times. Overall, birds made flexible decisions about danger by integrating personal and social information, while weighing information relevance. These findings support the idea that a strategic balance of personal and social information could affect community function.
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Reação de Fuga , Comportamento Alimentar , Aves Canoras/fisiologia , Vocalização Animal , Animais , Território da Capital Australiana , Comportamento PredatórioRESUMO
Species facing similar selection pressures should recognize heterospecific alarm signals. However, no study has so far examined heterospecific alarm-call recognition in response to parasitism by cuckoos. In this study, we tested whether two sympatric host species of the common cuckoo Cuculus canorus, Oriental reed warbler Acrocephalus orientalis (ORW, main host), and black-browed reed warbler Acrocephalus bistrigiceps (BRW, rare host), could recognize each other's alarm calls in response to cuckoos. Dummies of common cuckoo (parasite) and Eurasian sparrowhawk Accipiter nisus (predator) were used to induce and record alarm calls of the two warbler species, respectively. In the conspecific alarm-call playback experiments, ORW responded more strongly to cuckoo alarm calls than to sparrowhawk alarm calls, while BRW responded less strongly to cuckoo alarm calls than to sparrowhawk alarm calls. In the heterospecific alarm-call playback experiments, both ORW and BRW responded less strongly to cuckoo alarm calls than sparrowhawk alarm calls. BRW seemed to learn the association between parasite-related alarm calls of the ORW and the cuckoo by observing the process of ORW attacking cuckoos. In contrast, alarm calls of BRW to cuckoos were rarely recorded in most cases. BRW with low parasite pressure still developed recognition of heterospecific parasite-related alarm call. Unintended receivers in the same community should recognize heterospecific alarm calls precisely to extract valuable information.
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Passeriformes , Aves Canoras , Animais , Comportamento de Nidação , Reconhecimento PsicológicoRESUMO
When they detect a predator, many species emit anti-predator vocalizations. In some cases, they emit mobbing calls, which are associated with the caller approaching and harassing the predator while attracting others to join it. Surprisingly, although mobbing has been widely reported in adults of numerous species, there has been no test of the role of learning in mobbing call recognition, especially during ontogeny. Here, we exposed wild great tit (Parus major) nestlings to playbacks of an unthreatening novel sound either associated with conspecific mobbing calls (experimental treatment) or with another unthreatening novel sound (control treatment). We then tested them as nestlings and fledglings to see how they respond to the novel sound compared to conspecific mobbing calls. Results revealed that fledglings in the experimental treatment behaved similarly to conspecific mobbing calls and the novel sound associated with conspecific mobbing calls. Because mobbing efficiency is often linked to interspecific communication, associative learning should be used by heterospecifics as mobbing calls recognition mechanism. Regardless of treatment during the nestling phase, fledglings always were sensitive to the playback of conspecific mobbing calls. However, fledglings from the control group were more likely to approach the loudspeaker than those from the experimental group when mobbing calls were played suggesting that overexposure during the nestling phase altered mobbing learning. Overall, these results suggest that learning could play a role in the recognition of calls, like heterospecific mobbing calls, when paired with conspecific mobbing, and that mobbing is perceived as a threatening stimulus from a very young age.
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Bullying , Passeriformes , Animais , Condicionamento Clássico , Aprendizagem , Vocalização AnimalRESUMO
Japanese tits (Parus minor) produce specific alarm calls when they encounter a predatory snake. A recent field experiment showed that receiver tits became visually perceptive to an object resembling a snake when hearing these calls. However, the tits did not respond to the same object when hearing other call types or when the object was dissimilar to a snake. These findings provide the first experimental evidence for the retrieval of a visual search image from specific alarm calls, offering a novel approach for investigating the cognitive mechanisms underlying referential communication in wild animals.
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Aves , Percepção Visual , Vocalização Animal , Animais , Animais SelvagensRESUMO
The snake alarm call of Japanese tits prompts nesting adults to search for and mob the reptile until it is driven away. From playback experiments, Suzuki (2018) has inferred that the call provides an associative cue, evoking a searching image of the salient visual features of the predator-a novel approach to exploring visual attention and vocal communication in the wild.
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Vocalização Animal , AnimaisRESUMO
In many primates, the acoustic properties of alarm calls can provide information on the level of perceived predatory threat as well as influence the antipredator behavior of nearby conspecifics. The present study examined the harmonics-to-noise ratio (tonality of spectral structure) of alarm calls emitted by white-faced capuchin monkeys (Cebus capucinus) in trees directed at photographic models of a boa constrictor, neotropical rattlesnake, scorpion eater snake, and white snake-shaped control presented on the ground. The average and peak harmonics-to-noise ratios of initial alarm calls by infants, juveniles, and adults and those of nearby second callers were analyzed using PRAAT software. Averaged for age class, the peak harmonics-to-noise ratio of alarm calls directed at the boa constrictor model, characterizing a primary capuchin predator, was reliably higher than the peak harmonics-to-noise ratio of alarm calls directed at the harmless scorpion eater model. This effect was influenced by the higher harmonics-to-noise ratio of infant alarm calls and it disconfirmed our prediction, based on primate vocalization research, that snake perception would increase arousal and alarm-call noisiness. Levels of call tonality did not distinguish the boa and rattlesnake or rattlesnake and scorpion eater models for any age class. Higher alarm-call tonality appeared contagious to nearby perceivers, with focal alarm calling influencing the level of tonality of the first calls of second callers. Together, these findings suggest that the higher peak harmonics-to-noise ratio of capuchin alarm calling directed at snakes is contagious and possibly conveys information about the level of perceived predatory threat.
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Cebus capucinus/fisiologia , Serpentes , Vocalização Animal , Acústica , Fatores Etários , Animais , Cebus capucinus/crescimento & desenvolvimento , Costa Rica , Feminino , Masculino , Comportamento Predatório , Gravação em VídeoRESUMO
Vocal repertoires and call structure can provide insights into the behaviour and evolution of species, as well as aid in taxonomic classification. Nocturnal primates have large vocal repertoires. This suggests that acoustic communication plays an important role in their life histories. Little is known about the behavioural context or the intraspecific variation of their vocalisations. We used autonomous recording units and manual recorders to investigate the vocal behaviour and structure of loud calls of the small-eared greater galago (Otolemur garnettii)in Kenya and Tanzania. We describe the vocal repertoire, temporal calling patterns and structure of 2 loud calls of 2 subspecies: O. g. panganiensis and O. g. kikuyuensis. We found considerable intraspecific structural differences in both loud calls. These are congruent with the current subspecies classification. Differences in vocalisations among populations are not consistent with the "acoustic adaptation hypothesis," rather they are likely a result of geographic variation due to isolation caused by vegetational barriers in southern Kenya.