Investigating Individual Vocal Signatures and Small-Scale Patterns of Geographic Variation in Female Bornean Gibbon (<Emphasis Type="Italic">Hylobates muelleri</Emphasis>) Great Calls

Quantifying patterns of variation in primate vocalizations has important implications for understanding the evolutionary processes that lead to variation in phenotypic traits more broadly. Here, we investigated individuality and patterns of geographic variation across a small geographic scale (ca. 10 km) in female Bornean gibbon (Hylobates muelleri) great calls. We analyzed calls recorded from wild, unhabituated gibbon groups at the Stability of Altered Forest Ecosystems site in Sabah, Malaysia. We estimated 23 acoustic features in 376 great calls from 33 different females. We used linear discriminant function analysis to investigate intra- and interindividual variation in great calls. To examine small-scale patterns of geographic variation great calls we investigated measures of acoustic dissimilarity as a function of distance. We found that temporal features (such as the duration of the notes and the duration of rest between notes) contributed substantially to individuality. We were able to identify females based on their calls with 95.7% accuracy using leave-one-out cross-validation. We found no discernible patterns of geographic variation at our site; females with neighboring territories were just as likely to have similar calls as females with more distant territories. It is possible that we did not sample across a large enough geographic range, or that substantial interindividual variation effectively swamped across-site patterns of variation. Our findings add to the growing body of evidence for individual vocal signatures in primates and mammals, but further research is needed to understand the evolutionary mechanisms that contribute to individuality in gibbon calls.     

Evidence for High Variability in Temporal Features of the Male Coda in Müller’s Bornean Gibbons (<Emphasis Type="Italic">Hylobates muelleri</Emphasis>)

Most pair-living primate species engage in duets, wherein males and females produce coordinated vocalizations. Previous analyses of male gibbon contributions to the duet have shown that calls are individually distinct. Here we investigate variation in the temporal and spectral parameters in the male contribution to the duet, also known as the coda, of wild, nonhabituated male Müller’s Bornean gibbons (Hylobates muelleri), recorded both opportunistically and as a response to playbacks at the Stability of Altered Forest Ecosystems site in Sabah, Malaysia. We used linear discriminant function analysis to estimate the intra- and interindividual variation in 13 spectral and temporal parameters of the vocalizations (N?=?337) of 31 male gibbons. To further understand how call features vary within and between individuals we used a multivariate, variance components model to investigate how variance in features was partitioned at these two levels. We could identify males with a 66% accuracy using leave-one-out cross-validation, a relatively low score compared to female Müller’s Bornean gibbons and males of other species. We found that for some features (such as maximum frequency of the notes) most of the variance occurred between males, but for others (specifically total duration of the call and duration of rest in between notes) most of the variance occurred within a single male. Overall, male Müller’s Bornean gibbon coda vocalizations showed greater variability relative to their female counterparts, raising questions about potential differences in the function of the male and female contributions to the duet in Müller’s Bornean gibbons and the gibbon taxon as a whole.     

Macrogeographical variability in the great call of Hylobates agilis: assessing the applicability of vocal analysis in studies of fine‐scale taxonomy of gibbons

Vocal characteristics have been used extensively to distinguish different taxonomic units of gibbons (family Hylobatidae). The agile gibbon (Hylobates agilis) has a disjunct distribution range in the Southeast Asian archipelago (remnants of the former Sunda landmass), and populations on different islands are currently recognized as distinct subspecies or even species. We recorded great calls from female agile gibbons from two populations on Sumatra and two populations on Borneo and examined the vocal variability on four levels: within‐individuals, between‐individuals, between‐populations and between‐islands. The primary objective was to evaluate the effect of geographical isolation on variability in song pattern and to test whether proposed island‐specific song characteristics exist, reflecting evolutionary divergence between Sumatran and Bornean agile gibbons. One hundred great calls were recorded from 20 females and analyzed for 18 spectral and temporal acoustic parameters. Principal component analysis followed by a nested ANOVA on components revealed a complex pattern of song variability not likely to reflect taxonomic or evolutionary relationship. We found no evidence that Sumatran and Bornean agile gibbons have evolved different vocal characteristics, refuting a distinction between them based on vocal characteristics. A high level of plasticity was found in great calls from the same individual, and generally the inferred pattern of variability suggested that ecological or social factors may confound any genetically based island dialects. Am. J. Primatol. 72:142–151, 2010. © 2009 Wiley‐Liss, Inc.     

Advertising individual identity by mother and adolescent contact calls in Siberian wapiti Cervus elaphus sibiricus

Individualistic contact calls facilitate mother‐offspring reunion after separation. However, in many mammals, both the acoustic structure and individuality of contact calls differ between mother and young. In contrast, in Siberian wapiti Cervus elaphus sibiricus, contact calls are similar in the acoustics between mother and young, whereas effects of this similarity on vocal individuality were not investigated. In this study, we analyzed acoustic differences between closed‐mouth (nasal) and open‐mouth (oral) contact calls and examined individuality of the most usual oral calls of 19 Siberian wapiti (9 hinds and 10 5–6‐month adolescents) emitted in response to mother‐offspring separation. In the oral calls, the values of frequency and power variables were higher than in the nasal calls. Calls of hinds and adolescents did not differ by the maximum fundamental frequency and duration, whereas the peak frequency was higher in the young. Discriminant function analysis (DFA) based on 11 acoustic variables of oral calls accurately classified to individual 92.5% of hind calls and 96.9% of adolescent calls (chi‐square test for differences between hinds and adolescents, p = 0.19). Variables mainly contributing to vocal identity (duration, start, and maximum fundamental frequency) were the same in calls of mothers and adolescents. We conclude that similarities in the acoustics calls of mothers and adolescents mean that they do not differ in their potential for encoding individual identity, suggesting a mutual process of mother‐offspring vocal recognition in Siberian wapiti.     

The ontogeny of acoustic individuality in the nasal calls of captive goitred gazelles, Gazella subgutturosa

Individualistic voices are important for establishing personalized relationships among individuals. In young animals, individual vocal identity is affected by permanent changes of the acoustics due to the growth of their vocal apparatus. Different acoustic variables change uncoordinatedly, so vocal individuality should be repeatedly upgraded along development. We compared classifying accuracy of individuals and sexes by nasal calls in fast-growing goitred gazelles Gazella subgutturosa at two ontogenetic stages, juvenile (3-6 weeks of age) and adolescent (23-26 weeks of age). Juvenile "spring" nasal calls and adolescent "fall" nasal calls were examined in the same 35 calves (18 males, 17 females), wild-born in May and then hand-raised. Discriminate function analysis based on four formants, fundamental frequency, duration and three power quartiles, revealed an equally high potential of spring and fall calls to encode sex. The individuality was very high in both ages but significantly higher in fall calls. Classifying calls to individuals was based on the same three acoustic variables (fundamental frequency and third and fourth formants) in both ages, although their actual values changed uncoordinatedly from spring to fall in most subjects. Our results suggest updating acoustic individuality in nasal calls of adolescent goitred gazelles accordingly to the newly emerged acoustic variation.     

A comparison of individual distinctiveness in three vocalizations of the dwarf mongoose (Helogale parvula)

Individual specificity can be found in the vocalizations of many avian and mammalian species. However, it is often difficult to determine whether these vocal cues to identity rise from “unselected” individual differences in vocal morphology or whether they have been accentuated by selection for the purposes of advertising caller identity. By comparing the level of acoustic individuality of different vocalizations within the repertoire of a single species, it is possible to ascertain whether selection for individual recognition has modified the vocal cues to identity in particular contexts. We used discriminant function analyses to determine the level of accuracy with which calls could be classified to the correct individual caller, for three dwarf mongoose (Helogale parvula) vocalizations: contact, snake, and isolation calls. These calls were similar in acoustic structure but divergent in context and function. We found that all three call types showed individual specificity but levels varied with call type (increasing from snake to contact to isolation call). The individual distinctiveness of each call type appeared to be directly related to the degree of benefit that signalers were likely to accrue from advertising their identity within that call context. We conclude that dwarf mongoose signalers have undergone selection to facilitate vocal individual recognition, particularly in relation to the species’ isolation call.     

Individuality of distress and discomfort calls in neonates with bass voices: Wild‐living goitred gazelles (Gazella subgutturosa) and saiga antelopes (Saiga tatarica)

Neonate ruminants produce distress calls when captured by a predator and discomfort milk begging calls when hungry. In many neonate ruminants, the distress and discomfort calls are high‐frequency vocalizations, in which the fundamental frequency is the key variable for recognition of their emotional arousal by caregivers. In contrast, in this study, we examine the low‐frequency open‐mouth distress and discomfort calls in the neonates of two species of wild‐living ungulates, which clearly highlight vocal tract resonances (formants). In the goitred gazelle (Gazella subgutturosa), the distress calls were higher in fundamental frequency (f0) and in the first and third formants than the discomfort calls. The accuracy of classifying individuals by variables of distress calls with discriminant function analysis (67%) was significantly lower than that of discomfort calls (85%). In the saiga (Saiga tatarica), only the third formant was higher in the distress calls than in the discomfort calls. The accuracy of classifying individuals by variables of distress calls (89%) did not differ significantly from that of discomfort calls (94%). Thus, the use of acoustic cues to vocal identity and to the degree of arousal differs between the two species. Calls were significantly more individualistic in the saiga, probably because this species lives in large herds and neonates use a ‘following’ antipredatory strategy, in which vocal individuality is crucial for mother–offspring communication. In contrast, goitred gazelles live in smaller groups and neonates use a ‘hiding’ antipredatory strategy. Accordingly, mothers can rely on additional environmental cues for spotting their young and this may decrease the necessity for individualization of the calls of neonates.     

Individuality in the vocalizations of infant and adult coppery titi monkeys (Plecturocebus cupreus)

As social animals, many primates use acoustic communication to maintain relationships. Vocal individuality has been documented in a diverse range of primate species and call types, many of which have presumably different functions. Auditory recognition of one's neighbors may confer a selective advantage if identifying conspecifics decreases the need to participate in costly territorial behaviors. Alternatively, vocal individuality may be nonadaptive and the result of a unique combination of genetics and environment. Pair-bonded primates, in particular, often participate in coordinated vocal duets that can be heard over long distances by neighboring conspecifics. In contrast to adult calls, infant vocalizations are short-range and used for intragroup communication. Here, we provide two separate but complementary analyses of vocal individuality in distinct call types of coppery titi monkeys (Plecturocebus cupreus) to test whether individuality occurs in call types from animals of different age classes with presumably different functions. We analyzed 600 trill vocalizations from 30 infants and 169 pulse-chirp duet vocalizations from 30 adult titi monkeys. We predicted that duet contributions would exhibit a higher degree of individuality than infant trills, given their assumed function for long-distance, intergroup communication. We estimated 7 features from infant trills and 16 features from spectrograms of adult pulse-chirps, then used discriminant function analysis with leave-one-out cross-validation to classify individuals. We correctly classified infants with 48% accuracy and adults with 83% accuracy. To further investigate variance in call features, we used a multivariate variance components model to estimate variance partitioning in features across two levels: within- and between-individuals. Between-individual variance was the most important source of variance for all features in adults, and three of four features in infants. We show that pulse-chirps of adult titi monkey duets are individually distinct, and infant trills are less individually distinct, which may be due to the different functions of the vocalizations.     

Note-, phrase- and song-specific acoustic variables contributing to the individuality of male duet song in the Bornean southern gibbon (Hylobates albibarbis)

In this study, we examine acoustic individuality in male duet songs of wild, non-habituated Bornean southern gibbons (Hylobates albibarbis) and identify contributing acoustic variables. We recorded 174 male duet songs from nine groups in a rainforest in Central Kalimantan, Indonesia. Each male portion of the duet was analysed for 14 acoustic variables at three levels of variation, including six note-specific variables (start frequency, end frequency, minimum frequency, maximum frequency, average frequency and duration), four phrase-specific variables (minimum frequency, maximum frequency, duration and number of syllables) and four song-specific variables (minimum frequency, maximum frequency, duration and number of syllables). Principal component analysis was performed to summarise each of these sets of variables into a total of six principal components (PCs). Strong acoustic individuality was found in all PCs and at all three levels: note, phrase and song (all p < 0.001). Furthermore, a particularly high magnitude of individuality was found in PC 1 of the song-specific analysis, defined by the acoustic variables of duration and number of syllables. Due to the high levels of individuality, we suggest that these acoustic variables may be used by Bornean southern gibbons for individual discrimination. As well as furthering our biological understanding of male gibbon song with regards to individuality and associated conspecific recognition, these findings also have the potential to help improve population survey methods, such as the acoustic sampling method using listening points, by offering a more accurate method of individual recognition.     

Acoustic features contributing to the individuality of wild agile gibbon (Hylobates agilis agilis) songs

We examined acoustic individuality in wild agile gibbon Hylobates agilis agilis and determined the acoustic variables that contribute to individual discrimination using multivariate analyses. We recorded 125 female-specific songs (great calls) from six groups in west Sumatra and measured 58 acoustic variables for each great call. We performed principal component analysis to summarize the 58 variables into six acoustic principal components (PCs). Generally, each PC corresponded to a part of the great call. Significant individual differences were found across six individual gibbons in each of the six PCs. Moreover, strong acoustic individuality was found in the introductory and climax parts of the great call. In contrast, the terminal part contributed little to individual identification. Discriminant analysis showed that these PCs contributed to individual discrimination with high repeatability. Although we cannot conclude that agile gibbon use these acoustic components for individual discrimination, they are potential candidates for individual recognition.     

Vocal and Optical Indicators of Individual Quality in a Social Seabird,the Crested Auklet (Aethia cristatella)

Indicators of individual quality in ornamentation or in vocalizations have been reported for different animal species. However, no studies have jointly investigated ornamentation and vocalizations in one species. The crested auklet (Aethia cristatella, Alcidae) is a small colonial seabird of the North Pacific and is unusual for a bird in using optical, vocal, and olfactory signals. We estimated the potential for coding individual quality in vocalizations and plumage ornamentation and the relationship between vocal and optical traits in crested auklets. During the summer seasons of 2008–2009, we recorded 359 trumpet calls from 28 individually marked males and measured indices of body size, condition, and plumage patterns of 58 male and 48 female crested auklets from a breeding colony on Talan Island, Sea of Okhotsk. We found strong interindividual differences in trumpet call characteristics. Furthermore, we found that the maximum fundamental frequency of the loudest notes of the trumpet call is negatively correlated with body condition, and head crest length is positively correlated with body size. However, we found no relationship between vocal and ornamental traits. The results suggest that advertising calls of crested auklets signal caller individuality and quality, but future experimental studies should test whether or not this is indeed case.     

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

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

Significance of temporal and spectral acoustic cues for sexual recognition in Xenopus laevis

As in many anurans, males of the totally aquatic species, Xenopus laevis, advertise their sexual receptivity using vocalizations. Unusually for anurans, X. laevis females also advertise producing a fertility call that results in courtship duets between partners. Although all X. laevis calls consist of repetitive click trains, male and female calls exhibit sex-specific acoustic features that might convey sexual identity. We tested the significance of the carrier frequency and the temporal pattern of calls using underwater playback experiments in which modified calls were used to evoke vocal responses in males. Since males respond differently to male and female calls, the modification of a key component of sexual identity in calls should change the male's response. We found that a female-like slow call rhythm triggers more vocal activity than a male-like fast rhythm. A call containing both a female-like temporal pattern and a female-like carrier frequency elicits higher levels of courtship display than either feature alone. In contrast, a male-like temporal pattern is sufficient to trigger typical male-male encounter vocalizations regardless of spectral cues. Thus, our evidence supports a role for temporal acoustic cues in sexual identity recognition and for spectral acoustic cues in conveying female attractiveness in X. laevis.     

Long-distance communication of acoustic cues to social identity in African elephants

Research on long-distance vocal communication in mammals has tended to focus on the maximum distances over which a vocal signal might be physically detectable. For example, because elephants and some whales communicate using infrasonic calls, and low frequencies are particularly resilient to attenuation, it has often been assumed that these species can communicate over very long distances. However, a wide range of acoustic characteristics typically carry information on individual identity in mammalian calls, and frequency components crucial for social recognition could be distorted or lost as distance from the source increases. We used long-distance playback experiments to show that female African elephants, Loxodonta africana, can recognize a contact call as belonging to a family or bond group member over distances of 2.5 km, but that recognition is more usually achieved over distances of 1-1.5 km. We analysed female contact calls to distinguish source- and filter-related vocal characteristics that have the potential to code individual identity, and rerecorded contact calls 0.5-3.0 km from the loudspeaker to determine how different frequencies persist with distance. Our analyses suggest that the most important frequency components for long-distance communication of social identity may be well above the infrasonic range. When frequency components around 115 Hz become immersed in background noise, once propagation distances exceed 1 km, abilities for long-distance social recognition become limited. Our results indicate that the possession of an unusually long vocal filter, which appears to incorporate the trunk, may be a more important attribute for long-distance signalling in female African elephants than the ability to produce infrasound. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Who shall I say is calling? Validation of a caller recognition procedure in Bornean flanged male orangutan (Pongo pygmaeus wurmbii) long calls

Acoustic individual discrimination has been demonstrated for a wide range of animal taxa. However, there has been far less scientific effort to demonstrate the effectiveness of automatic individual identification, which could greatly facilitate research, especially when data are collected via an acoustic localization system (ALS). In this study, we examine the accuracy of acoustic caller recognition in long calls (LCs) emitted by Bornean male orangutans (Pongo pygmaeus wurmbii) derived from two data-sets: the first consists of high-quality recordings taken during individual focal follows (N = 224 LCs by 14 males) and the second consists of LC recordings with variable microphone-caller distances stemming from ALS (N = 123 LCs by 10 males). The LC is a long-distance vocalization. We therefore expect that even the low-quality test-set should yield caller recognition results significantly better than by chance. Automatic individual identification was accomplished using software originally developed for human speaker recognition (i.e. the MSR identity toolbox). We obtained a 93.3% correct identification rate with high-quality recordings, and 72.23% with recordings stemming from the ALS with variable microphone-caller distances (20–420 m). These results show that automatic individual identification is possible even though the accuracy declines compared with the results of high-quality recordings due to severe signal degradations (e.g. sound attenuation, environmental noise contamination, and echo interference) with increasing distance. We therefore suggest that acoustic individual identification with speaker recognition software can be a valuable tool to apply to data obtained through an ALS, thereby facilitating field research on vocal communication.     

Individuality in Corncrake Crex crex vocalizations

Vocal individuality has potential for the monitoring of bird species that are otherwise difficult to observe. In this study we assessed the potential of this technique for the monitoring of the globally threatened Corncrake Crex crex based on the analysis of calls recorded in Ireland and Scotland in 1993 and 1994. Discriminant function analysis correctly attributed >80% of individual calls based on five temporal parameters. A high level of individual distinctiveness was also found in the fine temporal structure of calls. When information on fine structure was added to the discriminant function analysis, classification of calls to individuals was improved to 100%. The structure of an individual's call was found to be consistent over the 2-year period. This study highlighted the problemsassociated with setting criteria for re-identifying individuals by calls. The consequences of these problems and the potential of vocal individuality for providing monitoring information in this species are discussed.     

Population differences and acoustic stability in male songs of wild western black crested gibbons (Nomascus concolor) in Mt. Wuliang, Yunnan

Population differences and acoustic stability in male songs of the western black crested gibbon (Nomascus concolor) at Mt. Wuliang, Yunnan, were investigated using data collected over 4 years. Detectable vocal differences were found between the western and eastern populations within Mt. Wuliang. Discriminant functions calculated using the phrases recorded in 2007-2008 correctly classified phrases recorded in 2009, and discriminant functions produced from phrases recorded in 2007-2009 could correctly classify phrases recorded in 2010 for 4 of 5 males. Results showed that the male songs of western black crested gibbons remain relatively stable over years. In light of the acoustic individuality in male songs of this gibbon species, which has recently been proved, and the acoustic stability shown in this research, we suggest that the song of male individuals may be useful in monitoring individuals or family groups of this species.     

基于MFCC和GMM的昆虫声音自动识别

昆虫的运动、 取食、 鸣叫都会发出声音, 这些声音存在种内相似性和种间差异性, 因此可用来识别昆虫的种类。基于昆虫声音的昆虫种类自动检测技术对协助农业和林业从业人员方便地识别昆虫种类非常有意义。本研究采用了语音识别领域里的声音参数化技术来实现昆虫的声音自动鉴别。声音样本经预处理后, 提取梅尔倒谱系数（Mel frequency cepstrum coefficient, MFCC）作为特征, 并用这些样本提取的MFCC特征集训练混合高斯模型（Gaussian mixture model, GMM）。最后用训练所得到的GMM对未知类别的昆虫声音样本进行分类。该方法在包含58种昆虫声音的样本库中进行了评估, 取得了较高的识别正确率（平均精度为98.95%）和较理想的时间性能。该测试结果证明了基于MFCC和GMM的语音参数化技术可以用来有效地识别昆虫种类。     

Multimodal Signaling in Male and Female Foot-Flagging Frogs Staurois guttatus (Ranidae): An Alerting Function of Calling

In multimodal communication, individuals use several sensory modalities for information transfer. We report on novel observations of foot‐flagging in the Bornean ranid frog Staurois guttatus that is temporally linked to advertisement calling. In addition, we document the first case of foot‐flagging in a female anuran as well as additional visual displays in both males and females including arm‐waving, vocal‐sac pumping and open‐mouth display. In males, advertisement calls and foot‐flags were given throughout most of the day, suggesting that acoustic and visual signals form a multicomponent and multimodal display. We tested the efficacy‐based alerting signal hypothesis of multimodal communication using acoustic playback experiments with males. This hypothesis predicts that an initial signal draws the receiver's attention to the location of a subsequent more informative signal. Several lines of evidence supported the alerting hypothesis. First, the latency between foot‐flags and advertisement calls was significantly higher than that between advertisement calls and foot‐flags, suggesting a functional linkage with calls drawing attention to foot‐flags. Secondly, advertisement calling had a signaling function with males responding significantly more often with both calls and foot‐flags compared with pre‐ and post‐playback control periods. Finally, and most notably, all males tested turned towards the playback stimulus, suggesting that the advertisement call serves to focus their attention on subsequent signals. We discuss the potential of multimodal signaling for conspecific and heterospecific communication and the circumstances under which such a multimodal communication system could evolve.     

Individual Acoustic Variation in Fallow Deer (Dama dama) Common and Harsh Groans: A Source-Filter Theory Perspective

Mammals are able to distinguish conspecifics based on vocal cues, and the acoustic structure of mammal vocalizations is directly affected by the anatomy and action of the vocal apparatus. However, most studies investigating individual patterns in acoustic signals do not consider a vocal production‐based perspective. In this study, we used the source‐filter model of vocal production as a basis for investigating the acoustic variability of fallow deer groans. Using this approach, we quantified the potential of each acoustic component to carry information about individual identity. We also investigated if cues to individual identity carry over among the two groan types we describe: common and harsh groans. Using discriminant function analysis, we found that variables related to the fundamental frequency contour and the minimum frequencies of the highest formants contributed most to the identification of a given common groan. Common groans were individually distinctive with 36.6% (53.6% with stepwise procedure) of groans assigned to the correct individual. This level of discrimination is approximately six times higher than that predicted by chance. In addition, univariate anova s showed significant inter‐individual variation in the minimum formant frequencies when common and harsh groans were combined, suggesting that some information about individuality is shared between groan types. Our results suggest that the sound source and the vocal tract resonances act together to determine groan individuality and that enough variation exists to potentially allow individual recognition based on groans.