Unsupervised acoustic classification of individual gibbon females and the implications for passive acoustic monitoring

Passive acoustic monitoring (PAM) has the potential to greatly improve our ability to monitor cryptic yet vocal animals. Advances in automated signal detection have increased the scope of PAM, but distinguishing between individuals—which is necessary for density estimation—remains a major challenge. When individual identity is known, supervised classification techniques can be used to distinguish between individuals. Supervised methods require labelled training data, whereas unsupervised techniques do not. If the acoustic signals of individuals are sufficiently different, the number of clusters might represent the number of individuals sampled. The majority of applications of unsupervised techniques in animal vocalizations have focused on quantifying species‐specific call repertoires. However, with increased interest in PAM applications, unsupervised methods that can distinguish between individuals are needed. Here we use an existing dataset of Bornean gibbon female calls with known identity from five sites on Malaysian Borneo to test the ability of three different unsupervised clustering algorithms (affinity propagation, K‐medoids and Gaussian mixture model‐based clustering) to distinguish between individuals. Calls from different gibbon females are readily distinguishable using supervised techniques. For internal validation of unsupervised cluster solutions, we calculated silhouette coefficients. For external validation, we compared clustering results with female identity labels using a standard metric: normalized mutual information. We also calculated classification accuracy by assigning unsupervised cluster solutions to females based on which cluster had the highest number of calls from a particular female. We found that affinity propagation clustering consistently outperformed the other algorithms for all metrics used. In particular, classification accuracy of affinity propagation clustering was more consistent as the number of females increased, and when we randomly sampled females across sites. We conclude that unsupervised techniques may be useful for providing additional information regarding individual identity for PAM applications. We stress that although we use gibbons as a case study, these methods will be applicable for any individually distinct vocal animal.

[1]  Xin Jin,et al.  K-Means Clustering , 2010, Encyclopedia of Machine Learning.

[2]  R. Righini,et al.  Comparative Analysis of the Vocal Repertoire of Eulemur: A Dynamic Time Warping Approach , 2015, International Journal of Primatology.

[3]  Dena J. Clink,et al.  Evidence for High Variability in Temporal Features of the Male Coda in Müller’s Bornean Gibbons (Hylobates muelleri) , 2018, International Journal of Primatology.

[4]  C. Marshall,et al.  Has the Earth’s sixth mass extinction already arrived? , 2011, Nature.

[5]  Holger Klinck,et al.  Gibbons aren’t singing in the rain: presence and amount of rainfall influences ape calling behavior in Sabah, Malaysia , 2020, Scientific Reports.

[6]  R. Seyfarth,et al.  Vervets revisited: A quantitative analysis of alarm call structure and context specificity , 2015, Scientific Reports.

[7]  K. Hammerschmidt,et al.  Baboon vocal repertoires and the evolution of primate vocal diversity. , 2019, Journal of human evolution.

[8]  Brendan J. Frey,et al.  Non-metric affinity propagation for unsupervised image categorization , 2007, 2007 IEEE 11th International Conference on Computer Vision.

[9]  Adrian E. Raftery,et al.  Model-Based Clustering, Discriminant Analysis, and Density Estimation , 2002 .

[10]  Pengfei Fan,et al.  Individuality and Stability in Male Songs of Cao Vit Gibbons (Nomascus nasutus) with Potential to Monitor Population Dynamics , 2014, PloS one.

[11]  S. Malaivijitnond,et al.  Age related decline in female lar gibbon great call performance suggests that call features correlate with physical condition , 2016, BMC Evolutionary Biology.

[12]  J. Andrew Royle,et al.  Spatial capture–recapture with partial identity: An application to camera traps , 2018 .

[13]  Gaël Varoquaux,et al.  Scikit-learn: Machine Learning in Python , 2011, J. Mach. Learn. Res..

[14]  Hugo F. Posada-Quintero,et al.  Uniform Manifold Approximation and Projection for Clustering Taxa through Vocalizations in a Neotropical Passerine (Rough-Legged Tyrannulet, Phyllomyias burmeisteri) , 2020, Animals : an open access journal from MDPI.

[15]  C. Clark,et al.  Exploring movement patterns and changing distributions of baleen whales in the western North Atlantic using a decade of passive acoustic data , 2020, Global change biology.

[16]  Ulrich Bodenhofer,et al.  APCluster: an R package for affinity propagation clustering , 2011, Bioinform..

[17]  P M Kappeler,et al.  Social shaping of voices does not impair phenotype matching of kinship in mandrills , 2015, Nature Communications.

[18]  Tagaram Soni Madhulatha,et al.  Comparison between K-Means and K-Medoids Clustering Algorithms , 2011 .

[19]  T. Vu,et al.  An Application of Autonomous Recorders for Gibbon Monitoring , 2019, International Journal of Primatology.

[20]  J. Andrew Royle,et al.  Spatial capture–recapture for categorically marked populations with an application to genetic capture–recapture , 2019, Ecosphere.

[21]  Matthias Zeppelzauer,et al.  Towards an automated acoustic detection system for free-ranging elephants , 2015, Bioacoustics.

[22]  Beatriz de la Iglesia,et al.  Clustering Rules: A Comparison of Partitioning and Hierarchical Clustering Algorithms , 2006, J. Math. Model. Algorithms.

[23]  Arik Kershenbaum Review for "Unsupervised acoustic classification of individual gibbon females and the implications for passive acoustic monitoring" , 2020 .

[24]  J. Andrew Royle,et al.  Spatial Capture-Recapture for Categorically Marked Populations with An Application to Genetic Capture-Recapture , 2018, bioRxiv.

[25]  Stan Davis,et al.  Comparison of Parametric Representations for Monosyllabic Word Recognition in Continuously Spoken Se , 1980 .

[26]  P. McGregor,et al.  The role of vocal individuality in conservation , 2005, Frontiers in Zoology.

[27]  Leland McInnes,et al.  UMAP: Uniform Manifold Approximation and Projection for Dimension Reduction , 2018, ArXiv.

[28]  Hjalmar S. Kühl,et al.  Passive acoustic monitoring reveals group ranging and territory use: a case study of wild chimpanzees (Pan troglodytes) , 2016, Frontiers in Zoology.

[29]  Dena J. Clink,et al.  Evidence for vocal performance constraints in a female nonhuman primate , 2018, Animal Behaviour.

[30]  Murray G. Efford,et al.  Bird population density estimated from acoustic signals , 2009 .

[31]  Len Thomas,et al.  Estimating minke whale (Balaenoptera acutorostrata) boing sound density using passive acoustic sensors , 2013 .

[32]  Holger Klinck,et al.  Brevity is not a universal in animal communication: evidence for compression depends on the unit of analysis in small ape vocalizations , 2020, Royal Society Open Science.

[33]  T. Ishida,et al.  Short dispersal distance of males in a wild white-handed gibbon (Hylobates lar) population. , 2018, American journal of physical anthropology.

[34]  Delbert Dueck,et al.  Affinity Propagation: Clustering Data by Passing Messages , 2009 .

[35]  Corinna Cortes,et al.  Support-Vector Networks , 1995, Machine Learning.

[36]  Greg Hamerly,et al.  Accelerating Lloyd’s Algorithm for k -Means Clustering , 2015 .

[37]  Arik Kershenbaum,et al.  The Encoding of Individual Identity in Dolphin Signature Whistles: How Much Information Is Needed? , 2013, PloS one.

[38]  Hjalmar S. Kühl,et al.  Towards the automated detection and occupancy estimation of primates using passive acoustic monitoring , 2015 .

[39]  Christophe Boesch,et al.  Acoustic structure and variation in mountain and western gorilla close calls: a syntactic approach , 2014 .

[40]  David L. Borchers,et al.  A general framework for animal density estimation from acoustic detections across a fixed microphone array , 2015 .

[41]  Warren Y. Brockelman,et al.  Estimation of density of gibbon groups by use of loud songs , 1993, American journal of primatology.

[42]  Tao Guo,et al.  Adaptive Affinity Propagation Clustering , 2008, ArXiv.

[43]  Peter H. Wrege,et al.  Acoustic structure of forest elephant rumbles: a test of the ambiguity reduction hypothesis , 2019, Animal Cognition.

[44]  Dena J. Clink,et al.  Application of a semi-automated vocal fingerprinting approach to monitor Bornean gibbon females in an experimentally fragmented landscape in Sabah, Malaysia , 2019 .

[45]  Frank Kurth,et al.  Detecting bird sounds in a complex acoustic environment and application to bioacoustic monitoring , 2010, Pattern Recognit. Lett..

[46]  Teja Tscharntke,et al.  Autonomous sound recording outperforms human observation for sampling birds: a systematic map and user guide. , 2019, Ecological applications : a publication of the Ecological Society of America.

[47]  M. Picheny,et al.  Comparison of Parametric Representation for Monosyllabic Word Recognition in Continuously Spoken Sentences , 2017 .

[48]  Rizaldi,et al.  Possible Role of Mother-Daughter Vocal Interactions on the Development of Species-Specific Song in Gibbons , 2013, PloS one.

[49]  Ivo D. Dinov,et al.  k-Means Clustering , 2018 .

[50]  M. Brusco,et al.  Affinity propagation: An exemplar‐based tool for clustering in psychological research , 2019, The British journal of mathematical and statistical psychology.

[51]  Peter H. Wrege,et al.  Acoustic monitoring for conservation in tropical forests: examples from forest elephants , 2017 .

[52]  Huafu Chen,et al.  Analysis of activity in fMRI data using affinity propagation clustering , 2011, Computer methods in biomechanics and biomedical engineering.

[53]  D. Valente,et al.  Finding Meanings in Low Dimensional Structures: Stochastic Neighbor Embedding Applied to the Analysis of Indri indri Vocal Repertoire , 2019, Animals : an open access journal from MDPI.

[54]  Cristina Giacoma,et al.  The use of Artificial Neural Networks to classify primate vocalizations: a pilot study on black lemurs , 2009, American journal of primatology.

[55]  Dena J. Clink,et al.  Understanding sources of variance and correlation among features of Bornean gibbon (Hylobates muelleri) female calls. , 2018, The Journal of the Acoustical Society of America.

[56]  Seyed Omid Sadjadi,et al.  Who shall I say is calling? Validation of a caller recognition procedure in Bornean flanged male orangutan (Pongo pygmaeus wurmbii) long calls , 2017 .

[57]  Peter J. Rousseeuw,et al.  Finding Groups in Data: An Introduction to Cluster Analysis , 1990 .

[58]  Hiroto Enari,et al.  Feasibility assessment of active and passive acoustic monitoring of sika deer populations , 2017 .

[59]  Luca Scrucca,et al.  mclust 5: Clustering, Classification and Density Estimation Using Gaussian Finite Mixture Models , 2016, R J..

[60]  Lorenzo Picinali,et al.  Characterizing soundscapes across diverse ecosystems using a universal acoustic feature set , 2020, Proceedings of the National Academy of Sciences.

[61]  Dena J. Clink,et al.  Investigating Individual Vocal Signatures and Small-Scale Patterns of Geographic Variation in Female Bornean Gibbon (Hylobates muelleri) Great Calls , 2017, International Journal of Primatology.

[62]  Diego Llusia,et al.  Terrestrial Passive Acoustic Monitoring: Review and Perspectives , 2018, BioScience.

[63]  Vincent Nijman,et al.  Vegetation correlates of gibbon density in the peat‐swamp forest of the Sabangau catchment, Central Kalimantan, Indonesia , 2010, American journal of primatology.

[64]  I. Elamvazuthi,et al.  Voice Recognition Algorithms using Mel Frequency Cepstral Coefficient (MFCC) and Dynamic Time Warping (DTW) Techniques , 2010, ArXiv.

[65]  J. MacQueen Some methods for classification and analysis of multivariate observations , 1967 .

[66]  P. Tyack,et al.  Estimating animal population density using passive acoustics , 2012, Biological reviews of the Cambridge Philosophical Society.

[67]  K. Zuberbühler,et al.  Graded or discrete? A quantitative analysis of Campbell's monkey alarm calls , 2013, Animal Behaviour.

[68]  T. Q. Bartlett,et al.  Long‐term home range use in white‐handed gibbons (Hylobates lar) in Khao Yai National Park, Thailand , 2016, American journal of primatology.

[69]  Carel P van Schaik,et al.  Validation of an acoustic location system to monitor Bornean orangutan (Pongo pygmaeus wurmbii) long calls , 2015, American journal of primatology.

[70]  Lisette M. C. Leliveld,et al.  Acoustic correlates of individuality in the vocal repertoire of a nocturnal primate (Microcebus murinus). , 2011, The Journal of the Acoustical Society of America.

[71]  Marcelo Araya-Salas,et al.  warbleR: an r package to streamline analysis of animal acoustic signals , 2017 .

[72]  Sara C Keen,et al.  Automated detection of low-frequency rumbles of forest elephants: A critical tool for their conservation. , 2017, The Journal of the Acoustical Society of America.

[73]  Samara M. Haver,et al.  Humpback whales Megaptera novaeangliae alter calling behavior in response to natural sounds and vessel noise , 2018, Marine Ecology Progress Series.

[74]  Sidarta Ribeiro,et al.  Machine Learning Algorithms for Automatic Classification of Marmoset Vocalizations , 2016, PloS one.

[75]  Julie Gros-Louis,et al.  Selection for acoustic individuality within the vocal repertoire of wild chimpanzees , 1996, International Journal of Primatology.

[76]  Pengfei Fan,et al.  Effects of group density, hunting, and temperature on the singing patterns of eastern hoolock gibbons (Hoolock leuconedys) in Gaoligongshan, Southwest China , 2016, American journal of primatology.

[77]  Wen Xiao,et al.  Population Differences and Acoustic Stability in Male Songs of Wild Western Black Crested Gibbons (Nomascus concolor) in Mt. Wuliang, Yunnan , 2011, Folia Primatologica.

[78]  J. Mitani The behavioral regulation of monogamy in gibbons (Hylobates muelleri) , 1984, Behavioral Ecology and Sociobiology.

[79]  Delbert Dueck,et al.  Clustering by Passing Messages Between Data Points , 2007, Science.

[80]  R. Irizarry ggplot2 , 2019, Introduction to Data Science.

[81]  Derek Greene,et al.  Unsupervised Learning and Clustering , 2008, Machine Learning Techniques for Multimedia.

[82]  O. Friard,et al.  Unsupervised Acoustic Analysis of the Vocal Repertoire of the Gray-Shanked Douc Langur (Pygathrix cinerea) , 2017 .

[83]  David L. Borchers,et al.  An Efficient Acoustic Density Estimation Method with Human Detectors Applied to Gibbons in Cambodia , 2016, PloS one.

[84]  S. Malaivijitnond,et al.  Lar gibbon (Hylobates lar) great call reveals individual caller identity , 2015, American journal of primatology.

[85]  P. Mundinger,et al.  Animal cultures and a general theory of cultural evolution , 1980 .

[86]  Therese M. Donovan,et al.  Tools for automated acoustic monitoring within the R package monitoR , 2016 .

[87]  Sach Mukherjee,et al.  Temporal clustering by affinity propagation reveals transcriptional modules in Arabidopsis thaliana , 2010, Bioinform..

[88]  Andrew Zisserman,et al.  Very Deep Convolutional Networks for Large-Scale Image Recognition , 2014, ICLR.

[89]  S. Cheyne,et al.  Home range variation and site fidelity of Bornean southern gibbons [Hylobates albibarbis] from 2010-2018 , 2019, PloS one.

[90]  Jianwei Yuan,et al.  Comparative proteomic study reveals the enhanced immune response with the blockade of interleukin 10 with anti-IL-10 and anti-IL-10 receptor antibodies in human U937 cells , 2019, PloS one.

[91]  P. Rousseeuw Silhouettes: a graphical aid to the interpretation and validation of cluster analysis , 1987 .

[92]  M. Cugmas,et al.  On comparing partitions , 2015 .

[93]  K. Hammerschmidt,et al.  The Vocal Repertoire of Barbary Macaques: A Quantitative Analysis of a Graded Signal System , 2010 .

[94]  Daniel T. Larose,et al.  Discovering Knowledge in Data: An Introduction to Data Mining , 2005 .

[95]  K. Hammerschmidt,et al.  Characterizing Vocal Repertoires—Hard vs. Soft Classification Approaches , 2015, PloS one.

[96]  Klaus Zuberbühler,et al.  A method for automated individual, species and call type recognition in free-ranging animals , 2013, Animal Behaviour.

[97]  Richard M. Stern,et al.  Delta-spectral cepstral coefficients for robust speech recognition , 2011, 2011 IEEE International Conference on Acoustics, Speech and Signal Processing (ICASSP).

[98]  D. Rendall Acoustic correlates of caller identity and affect intensity in the vowel-like grunt vocalizations of baboons. , 2003, The Journal of the Acoustical Society of America.

[99]  D. Rendall,et al.  Vocal recognition of individuals and kin in free-ranging rhesus monkeys , 1996, Animal Behaviour.

[100]  T. Geissmann Duet‐splitting and the evolution of gibbon songs , 2002, Biological reviews of the Cambridge Philosophical Society.

[101]  E. Zimmermann,et al.  Paternal kin recognition in the high frequency / ultrasonic range in a solitary foraging mammal , 2012, BMC Ecology.

[102]  Yuan Yao,et al.  USING SONGS TO IDENTIFY INDIVIDUAL MEXICAN ANTTHRUSH FORMICARIUS MONILIGER: COMPARISON OF FOUR CLASSIFICATION METHODS , 2009 .

[103]  Michael J. Brusco,et al.  Examining the effect of initialization strategies on the performance of Gaussian mixture modeling , 2015, Behavior Research Methods.

[104]  J. Bezdek Numerical taxonomy with fuzzy sets , 1974 .

[105]  D. Cato,et al.  Cultural revolution in whale songs , 2000, Nature.