Nonlinearities in Meerkat Alarm Calls Prevent Receivers from Habituating

Despite the fact that nonlinearities are present in the calls of a number of different species, their adaptive function has received little empirical investigation. Previous studies have demonstrated that playbacks of nonlinear calls evoke a more extreme behavioural response and lead to an increase in responsiveness compared with control playbacks without nonlinearities. Consequently, it has been suggested that nonlinearities might prevent receivers from habituating, by increasing the unpredictability of the call (‘unpredictability hypothesis’). In this study, we tested the unpredictability hypothesis, specifically whether nonlinearities prevent receivers from habituating, by means of a playback experiment using meerkat (Suricata suricatta) alarm calls. We found that in meerkats, playbacks of naturally occurring nonlinear alarm calls take longer to habituate to than alarm calls without any nonlinear intrusions. These data provide important empirical support for the hypothesis that nonlinearities are not just an irrelevant by‐product of the vocal production system, but indeed function adaptively.     

大足鼠耳蝠交流声波非线性现象

非线性发声现象在动物的发声中普遍存在,因其具有进化上的意义而广受关注。非线性现象一般在动物激进状态下发出,可能具有一定的功能,然而国内外对蝙蝠非线性现象的研究集中于描述性的报道,缺乏进化功能上的探究。大足鼠耳蝠(Myotis pilosus)激进叫声包含2种音节类型,拱形调频音节(AFM)和噪音-短下调调频音节(NB-s DFM),能够组成3种叫声组合,只包含AFM的叫声组合(A)、只包含NB-s DFM的叫声组合(B)、既包含AFM又包含NB-s DFM的叫声组合(C),分别对应着没有非线性现象、具有非线性现象及一种过渡类型。通过回放3种叫声组合,记录7种具有代表性的行为反应(抬头、前臂移动、耳动、发出回声定位脉冲、震颤、张嘴、爬行)次数,其中,前臂移动和发出回声定位脉冲两种行为反应的结果显示,大足鼠耳蝠对上述3种叫声组合的反应程度有显著差异,即具有非线性现象的叫声组合(B)能够提高同种蝙蝠的反应程度。实验结果表明,蝙蝠发声中的非线性现象能够增强叫声的不可预测性,说明非线性现象在蝙蝠发声中可能具有功能上的适应性。     

Calls out of chaos: the adaptive significance of nonlinear phenomena in mammalian vocal production

Recent work on human vocal production demonstrates that certain irregular phenomena seen in human pathological voices and baby crying result from nonlinearities in the vocal production system. Equivalent phenomena are quite common in nonhuman mammal vocal repertoires. In particular, bifurcations and chaos are ubiquitous aspects of the normal adult repertoire in many primate species. Here we argue that these phenomena result from properties inherent in the peripheral production mechanism, which allows individuals to generate highly complex and unpredictable vocalizations without requiring equivalently complex neural control mechanisms. We provide examples from the vocal repertoire of rhesus macaques, Macaca mulatta, and other species illustrating the different classes of nonlinear phenomena, and review the concepts from nonlinear dynamics that explicate these calls. Finally, we discuss the evolutionary significance of nonlinear vocal phenomena. We suggest that nonlinear phenomena may subserve individual recognition and the estimation of size or fluctuating asymmetry from vocalizations. Furthermore, neurally ‘cheap’ unpredictability may serve the valuable adaptive function of making chaotic calls difficult to predict and ignore. While noting that nonlinear phenomena are in some cases probably nonadaptive by-products of the physics of the sound-generating mechanism, we suggest that these functional hypotheses provide at least a partial explanation for the ubiquity of nonlinear calls in nonhuman vocal repertoires.     

Acoustic structure of alarm calls in Indian sambar (<Emphasis Type="Italic">Rusa unicolor</Emphasis>) and Indian muntjac (<Emphasis Type="Italic">Muntiacus vaginalis</Emphasis>) in South Vietnam

The alarm call acoustic structure and nonlinear vocal phenomena of the Indian sambar (Rusa unicolor) and northern Indian muntjac (Muntiacus vaginalis) have been analyzed in detail as well as their vocal behavior in response to mobbing humans under natural conditions of southern Vietnam. The alarm calls of sambars, tonal barks separated by large intervals, were produced by animals standing on the place and gazing at a potentially dangerous object. Muntjacs flee off in danger and produced a series of dull barks interrupted with short intervals from a distance. The alarm call frequencies were characterized for sambars and muntjacs. The results of our study have been compared with the published data on alarm calls of other Cervidae species.     

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.     

Alarm call discrimination in a social rodent: adult but not juvenile degu calls induce high vigilance

Many social animals develop vocal communications to send and receive information efficiently in a group. In alarm communication, call recipients in a social group evaluate alarm calls, enhancing their probability of survival in the face of predatory threats. Calls from naïve and younger group members might be less evocative, in terms of rendering group members vigilant, than calls from more experienced adults because adults are generally more reliable. It remains uncertain, however, what acoustic characteristics render an alarm call reliable. Here, we report that adult degus, Octodon degus (Rodentia, Octodontidae), produced an alarm with a frequency-modulated (FM) syllable, accompanied by low bandwidth and entropy, to evoke a high-vigilance response amongst receivers. Unlike adults, subadult degus did not emit the FM syllable in the warning context, and their call without the FM syllable evoked less vigilance than the adult alarm. We suggest that the FM structure of the adult-produced syllable serves as the primary feature characterizing a reliable alarm call. Our results are consistent with those found in other social rodents, e.g., ground squirrels and gerbils, also produce FM alarm calls in high-urgency situations supports the importance of the FM syllable in alarm communication.     

非线性鸣声对雄性凹耳蛙应答的影响

为了解非线性鸣声对凹耳蛙(Odorrana tormota)应答音的影响以及非线性鸣声是否能够增强鸣声的不可预测性,本研究通过回放非线性鸣声和线性鸣声来刺激陌生雄性凹耳蛙,并记录应答次数及统计分析应答音相关参数。结果表明,回放非线性鸣声时会引起陌生蛙(n=22)更多次数的应答,但两种刺激引起的首次应答时间没有显著差异。对应答音相关参数分析表明,线性鸣声引起的应答音在总时长上比非线性鸣声引起的应答音更长且具有显著差异,而其他声音参数(包括平均基频、最大基频、最小基频、主频)均没有显著差异。推测当陌生雄蛙听到同类鸣叫时,出于保护领地和资源的本能反应,陌生蛙都会第一时间作出反应,因此在两类声音的应答反应时间上并没有区别。而在应答次数上,非线性鸣声引起了凹耳蛙更多次数的应答,可能是由于鸣声中的非线性现象使得声音更加复杂,包含更多信息,容易提高声音接收者对这类声音的关注度。本研究结果表明,凹耳蛙鸣声中包含的非线性现象能够增强其声音的不可预测性,引起陌生蛙产生更多的应答次数。     

Species-specific and shared features in vocal repertoires of three Eurasian ground squirrels (genus <Emphasis Type="Italic">Spermophilus</Emphasis>)

Along to alarm calls, Eurasian ground squirrels of the genus Spermophilus also produce other call types toward potential predators and rival conspecifics. Individually identified 50 speckled (Spermophilus suslicus), 18 European (S. citellus) and 59 yellow (S. fulvus) ground squirrels were examined for interspecies differences in their vocal repertoires. A separate sample of 116 (90 adult and 26 juvenile) S. suslicus was examined for presence of ultrasound in their alarm calls. In addition, all tonal calls in all the three species were checked for presence of nonlinear phenomena. Calls were elicited by approaching animals in live-traps or near burrows; some types of vocalizations were also recorded during handling. Eight call types, three tonal and five wideband ones, were described. Vocal repertoires were remarkably similar between species, excluding the alarm calls, which were species-specific. Alarm calls with ultrasonic components were found in two individuals of S. suslicus. Concerning nonlinear phenomena, biphonation in alarm calls of S. suslicus, frequency jumps and sidebands in screams of S. citellus, frequency jumps and subharmonics in screams of S. fulvus were found. Results are discussed with literature evidence on audible and ultrasonic vocalizations in ground squirrels.     

Bird calls: just emotional displays or something more?

Two widely held assumptions about the sounds of birds and other animals are (1) they are impulsive and involuntary, and cannot be controlled, and (2) they are based only on emotion, apparently because the stimuli eliciting them are thought to be very generalized. The validity of these assumptions has been tested in studies of the alarm calling and food calling behavior of domestic chickens. Videotapes of aerial and ground predators–a hawk overhead and a raccoon on the ground–were effective in eliciting the two major classes of alarm calls. The frequency of aerial alarm calling was strongly affected by presence or absence of a companion, while other aspects of antipredator behavior were unchanged. This so-called "audience effect" on calling is not found with the ground predator call, apparently because this call is addressed to the predator as well as companions. The rules for audience effects are different again with food calling. Evidently calling is not completely impulsive, but can be controlled. By varying the attributes of digitized video images of predators we have shown that stimuli eliciting the aerial predator alarm call are quite specific, encoding different information than the ground predator call. Playback experiments demonstrate that another chicken can decode this information, and react adaptively. Although emotion is undoubtedly involved in bird calling, we conclude that simple emotion-based models of bird calls are inadequate as the sole basis for explaining the vocal behavior of birds.     

Bird calls: just emotional displays or something more?

Two widely held assumptions about the sounds of birds and other animals are (1) they are impulsive and involuntary, and cannot be controlled, and (2) they are based only on emotion, apparently because the stimuli eliciting them are thought to be very generalized. The validity of these assumptions has been tested in studies of the alarm calling and food calling behavior of domestic chickens. Videotapes of aerial and ground predators–a hawk overhead and a raccoon on the ground–were effective in eliciting the two major classes of alarm calls. The frequency of aerial alarm calling was strongly affected by presence or absence of a companion, while other aspects of antipredator behavior were unchanged. This so-called "audience effect" on calling is not found with the ground predator call, apparently because this call is addressed to the predator as well as companions. The rules for audience effects are different again with food calling. Evidently calling is not completely impulsive, but can be controlled. By varying the attributes of digitized video images of predators we have shown that stimuli eliciting the aerial predator alarm call are quite specific, encoding different information than the ground predator call. Playback experiments demonstrate that another chicken can decode this information, and react adaptively. Although emotion is undoubtedly involved in bird calling, we conclude that simple emotion-based models of bird calls are inadequate as the sole basis for explaining the vocal behavior of birds.     

Ultrasound use by Sunda colugos offers new insights into the communication of these cryptic mammals

Recent reports of the use of ultrasound for communication by nocturnal mammals have expanded our understanding of behaviour in these animals. The vocal repertoire of colugos has so far only been known to include audible sound. Here, we report the use of ultrasound calls by Sunda colugos (Galeopterus variegatus, order Dermoptera). We recorded one type of call emitted by seven individuals with mean individual frequencies between 37.4 ± 0.6 and 39.2 ± 0.7 kHz during its maximum energy and lasting 28.7 ± 1.6 to 46.9 ± 21.1 ms. Each call showed 3–36 sequential pulses with individual mean interpulse intervals between 423.0 ± 101.4 and 1230.0 ± 315.4 ms. High frequency calls may serve as cryptic anti-predator alarm calls. Our observations suggest that more species of nocturnal mammals may use ultrasound to communicate, and that further studies are needed to determine the occurrence, function and diversity of these calls.     

Vocal repertoire of cooperatively breeding Smooth‐billed Anis

Calls are functionally diverse signals that mediate behavior in a wide variety of contexts in both passerines and non‐passerines. However, the call‐based acoustic communication systems of non‐passerines have received less attention from investigators than those of passerines. We examined the vocal repertoire of Smooth‐billed Anis (Crotophaga ani), cooperatively breeding cuckoos that live in groups with multiple breeding pairs. We recorded calls from 22 groups over two breeding seasons at the Cabo Rojo National Wildlife Refuge in Puerto Rico. We identified 11 call types and one group vocalization, and used an automated sound measurement program to quantify their acoustic features. Discriminant function analysis (DFA) correctly classified 74.2% of calls based on these features. The vocal repertoire of Smooth‐billed Anis is larger than that reported for the three other species in the subfamily Crotophaginae. Smooth‐billed Anis have at least two alarm calls, two nest‐specific calls, and one nest defense call. We also identified one possible signal of aggressive intent, one possible appeasement signal, and two calls that may communicate identity. The relatively large vocal repertoire of Smooth‐billed Anis and association of distinct call types with different functions and contexts supports the main prediction of the social complexity hypothesis, i.e., species with more complex social systems will have more complex communication systems.     

The Sound of Arousal: The Addition of Novel Non-linearities Increases Responsiveness in Marmot Alarm Calls

Vocal structure should reflect vocal function. While much attention has focused on quantifying attributes of harmonic vocalizations, the vocalizations of many species also may contain non-linear phenomena such as warbles, subharmonics, biphonation, and deterministic chaos or noise. The function of these non-linearities remains enigmatic. In some species, harmonic vocalizations abruptly become 'noisy' when individuals are physiologically aroused and the sudden onset of these non-linearities could signal arousal or fear to receivers. One untested functional hypothesis is that vocalizations containing non-linearities are more variable from one rendition to the next, and thus are harder to habituate to. In some situations, reducing the likelihood of habituation could be important. Signals that are highly evocative are more difficult to habituate to. Thus, we conducted playback experiments to foraging yellow-bellied marmots ( Marmota flaviventris ) to determine whether the addition of white noise (a non-linear acoustic phenomenon) to alarm calls elicited a greater response than control calls without the non-linearity or control calls with silence, rather than noise, added to them. Marmots spent less time foraging after hearing calls that included noise than after normal or control calls. This result is consistent with the unpredictability hypothesis and suggests that the adaptive value of non-linearities is to prevent habituation.     

Efficiency and Significance of Multiple Vocal Signals in Sibling Competition

Animals can compete for resources by displaying various acoustic signals that may differentially affect the outcome of competition. We propose the hypothesis that the most efficient signal to deter opponents should be the one that most honestly reveals motivation to compete. We tested this hypothesis in the barn owl (Tyto alba) in which nestlings produce more calls of longer duration than siblings to compete for priority access to the indivisible prey item their parents will deliver next. Because nestlings increase call rate to a larger extent than call duration when they become hungrier, call rate would signal more accurately hunger level. This leads us to propose three predictions. First, a high number of calls should be more efficient in deterring siblings to compete than long calls. Second, the rate at which an individual calls should be more sensitive to variation in the intensity of the sibling vocal competition than the duration of its calls. Third, call rate should influence competitors’ vocalization for a longer period of time than call duration. To test these three predictions we performed playback experiments by broadcasting to singleton nestlings calls of varying durations and at different rates. According to the first prediction, singleton nestlings became less vocal to a larger extent when we broadcasted more calls compared to longer calls. In line with the second prediction, nestlings reduced vocalization rate to a larger extent than call duration when we broadcasted more or longer calls. Finally, call rate had a longer influence on opponent’s vocal behavior than call duration. Young animals thus actively and differentially use multiple signaling components to compete with their siblings over parental resources.     

四川梅花鹿产仔换茸期声行为的研究

2009年4～9月在四川省若尔盖县铁布自然保护区,对四川梅花鹿Cervusnippon sichuanicus产仔换茸期的声行为进行了较系统的研究。四川梅花鹿产仔换茸期的声行为可以分为报警声、惊叫声、吼叫声、母子召唤声等20种鸣声。通过声谱分析获得了各种鸣声的语谱图及其频谱特征,并通过野外观察初步确定了这些声行为的生物学意义。在遇到危险或潜在危险时,成年雄鹿往往第一个发出报警鸣声,而雌鹿的报警声大约是雄鹿的两倍多。成年个体的主动防御鸣声频次要多于亚成体,而幼体未见有该类鸣声。对梅花鹿不同亚种和不同季节的几种声行为进行了比较。     

Investigating the potential for call combinations in a lifelong vocal learner

The ability for humans to create seemingly infinite meaning from a finite set of sounds has likely been a critical component in our success as a species, allowing the unbounded communication of information. Syntax, the combining of meaningful sounds into phrases, is one of the primary features of language that enables this extensive expressivity. The evolutionary history of syntax, however, remains largely debated, and it is only very recently that comparative data for syntax in animals have been revealed. Here, we provide further evidence for a structural basis of potential syntactic‐like call combinations in the vocal communication system of a group‐living songbird. Acoustic analyses indicate that Western Australian magpies (Gymnorhina tibicen dorsalis) structurally combine generic alarm calls with acoustically distinct alert calls to produce an alarm alert sequence. These results are distinct from previous examples of call combinations as, to our knowledge, evidence for this capacity is yet to be demonstrated in the natural communication of a non‐human species that is capable of vocal learning throughout life. These findings offer prospects for experimental investigation into the presence and function of magpie call combinations, extending our understanding of animal vocal complexity.     

Semantic Differences in Sifaka (Propithecus verreauxi) Alarm Calls: A Reflection of Genetic or Cultural Variants?

In this study, we compared the usage of alarm calls and anti‐predator strategies between a captive and a wild lemur population. The wild lemur population was studied earlier in Western Madagascar ( Fichtel & Kappeler 2002 ). The captive population was studied in outdoor enclosures of the Duke University Primate Center. Alarm calls and anti‐predator behavior were elicited by conducting experiments with both vocal and visual dummies. We scored the subjects’ immediate behavioral responses, including alarm calls, from video recordings made during the experiments. In principle, both populations have a mixed alarm call system with functionally referential alarm calls for aerial predators and general alarm calls for terrestrial and aerial predators and for situations associated with high arousal, such as group encounters. Although wild and captive sifakas exhibit the same alarm call system and use the same alarm call types, we discovered striking differences in the usage and perception of some of the alarm calls. We argue that these differences indicate either an evolutionary drift in the meaning of these calls or reflect cultural variation. The latter possibility is consistent with our understanding of the ontogeny of call usage and comprehension.     

Effect of alarm calling by male Red‐winged Blackbirds on nestling begging and female provisioning behavior

ABSTRACT Nestling begging and parental provisioning can attract nest predators and reduce reproductive success, so parents and their offspring might be expected to respond adaptively by minimizing predator‐attracting cues when predators threaten nests. Male Red‐winged Blackbirds (Agelaius phoeniceus) are well known for their antipredator alarm calls that contain information about the approach of potential nest predators. We examined the begging behavior of nestlings and the provisioning behavior of females in response to antipredator alarm calls of males to test the adaptive response hypothesis. Playback experiments provided no evidence that alarm calls function to switch off vocal begging; nestlings were equally likely to beg vocally during playback and control periods. Video recordings showed that male alarm calling had no significant effect on inappropriate vocal begging (in the absence of an adult), but significantly reduced the incidence of spontaneous calling (in the absence of begging). Adult females responded to male antipredator alarm calls by delaying their provisioning visits. In addition, although having no significant effect on use of nest‐arriving calls by females, male alarm calling significantly reduced their use of nest‐leaving calls. We conclude that nestling and female Red‐winged Blackbirds respond to male alarm calls in ways that might reduce the risk of predation, but nestlings beg vocally when females arrive to feed them, regardless of male alarm calling, perhaps to avoid a competitive disadvantage with broodmates.     

Female Putty-Nosed Monkeys Use Experimentally Altered Contextual Information to Disambiguate the Cause of Male Alarm Calls

Many animal vocal signals are given in a wide range of contexts which can sometimes have little in common. Yet, to respond adaptively, listeners must find ways to identify the cause of a signal, or at least rule out alternatives. Here, we investigate the nature of this process in putty-nosed monkeys, a forest primate. In this species, adult males have a very restricted repertoire of vocalizations which are given in response to a wide variety of events occurring under conditions of limited visibility. We carried out a series of field playback experiments on females (N = 6) in a habituated group in Gashaka Gumti National Park, Nigeria, in which male alarm/loud calls were presented either alone, or following acoustic information that simulated the occurrence of natural disturbances. We demonstrate that listeners appear to integrate contextual information in order to distinguish among possible causes of calls. We conclude that, in many cases, pragmatic aspects of communication play a crucial role in call interpretation and place a premium on listeners'' abilities to integrate information from different sources.