Identification of behaviours from accelerometer data in a wild social primate

BackgroundThe use of accelerometers in bio-logging devices has proved to be a powerful tool for the quantification of animal behaviour. While bio-logging techniques are being used on wide range of species, to date they have only been seldom used with non-human primates. This is likely due to three main factors: the long tradition of direct field observations, a difficulty of attaching bio-logging devices to wild primates and the challenge of deciphering acceleration signals in species’ with remarkable locomotor and behavioural diversity. Here, we overcome these aforementioned obstacles and provide methodology for identification of behaviours from accelerometer data of wild chacma baboons (Papio ursinus) in Cape Town, South Africa.ResultsWe apply machine learning techniques to process complex accelerometer data, collected by bespoke tracking collars to quantify a range of behaviours (focusing on locomotion and foraging behaviour). We successfully identify six broad state behaviours that represent 93.3% of the time budget of the baboons. Resting, walking, running and foraging were all identified with high recall and precision representing the first classification of multiple behavioural states from accelerometer data for a wild primate.ConclusionOur ‘end to end’ process—from collar design and build to the collection and quantification of acceleration data—provides advantages over gathering data by traditional observation, not least because it affords data collection without the presence of an observer which may affect an animal’s behaviour. Furthermore, our methodology and findings open new possibilities for the fine-scale study of movement and foraging ecology in wild primates, and in particular our baboon study population which is in conflict with people.

[1]  Andrew J. King,et al.  Dominance and Affiliation Mediate Despotism in a Social Primate , 2008, Current Biology.

[2]  E. Shepard Identification of animal movement patterns using tri-axial accelerometry , 2008 .

[3]  Rory P. Wilson,et al.  Tri-Axial Dynamic Acceleration as a Proxy for Animal Energy Expenditure; Should We Be Summing Values or Calculating the Vector? , 2012, PloS one.

[4]  S. Bortolamiol,et al.  Wild Chimpanzees on the Edge: Nocturnal Activities in Croplands , 2014, PloS one.

[5]  Steven D. Prager,et al.  The dynamics of animal social networks: analytical, conceptual, and theoretical advances , 2014 .

[6]  K. Strier Long‐term field studies: positive impacts and unintended consequences , 2010, American journal of primatology.

[7]  L. Naughton-Treves Predicting Patterns of Crop Damage by Wildlife around Kibale National Park, Uganda , 1998 .

[8]  Noureddine Manamanni,et al.  Posture and body acceleration tracking by inertial and magnetic sensing: Application in behavioral analysis of free-ranging animals , 2011, Biomed. Signal Process. Control..

[9]  Andrew J. King,et al.  All together now: behavioural synchrony in baboons , 2009, Animal Behaviour.

[10]  J. Altmann,et al.  Observational study of behavior: sampling methods. , 1974, Behaviour.

[11]  S. Wanless,et al.  Can Ethograms Be Automatically Generated Using Body Acceleration Data from Free-Ranging Birds? , 2009, PloS one.

[12]  R. A. Hill,et al.  Market forces predict grooming reciprocity in female baboons , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[13]  Andy Liaw,et al.  Classification and Regression by randomForest , 2007 .

[14]  Willem Bouten,et al.  Optimizing acceleration-based ethograms: the use of variable-time versus fixed-time segmentation , 2014, Movement ecology.

[15]  Robin I. M. Dunbar,et al.  Time: a hidden constraint on the behavioural ecology of baboons , 1992, Behavioral Ecology and Sociobiology.

[16]  E. L. C. Shepard,et al.  Can accelerometry be used to distinguish between flight types in soaring birds? , 2015, Animal Biotelemetry.

[17]  M. O’Riain,et al.  The Spatial Ecology of Chacma Baboons (Papio ursinus) in a Human-modified Environment , 2011, International Journal of Primatology.

[18]  E. V. van Loon,et al.  From Sensor Data to Animal Behaviour: An Oystercatcher Example , 2012, PloS one.

[19]  Cédric Sueur,et al.  A Non-Lévy Random Walk in Chacma Baboons: What Does It Mean? , 2011, PloS one.

[20]  K. Yoda,et al.  Precise monitoring of porpoising behaviour of Adélie penguins determined using acceleration data loggers. , 1999, The Journal of experimental biology.

[21]  Stephen A. Ellwood,et al.  Use of tri-axial accelerometers to assess terrestrial mammal behaviour in the wild. , 2016 .

[22]  L. Dubroca,et al.  Slowness and acceleration: a new method to quantify the activity budget of chelonians , 2008, Animal Behaviour.

[23]  Leo Breiman,et al.  Random Forests , 2001, Machine Learning.

[24]  Robin I. M. Dunbar,et al.  Group size, grooming and social cohesion in primates , 2007, Animal Behaviour.

[25]  R. Byrne,et al.  Dietary and foraging strategies of baboons. , 1991, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[26]  J. Pruetz,et al.  Giving the Forest Eyes: The Benefits of Using Camera Traps to Study Unhabituated Chimpanzees (Pan troglodytes verus) in Southeastern Senegal , 2014, International Journal of Primatology.

[27]  Akinori Takahashi,et al.  Linking animal-borne video to accelerometers reveals prey capture variability , 2013, Proceedings of the National Academy of Sciences.

[28]  E. Fernández‐Duque,et al.  Cathemerality and Lunar Periodicity of Activity Rhythms in Owl Monkeys of the Argentinian Chaco , 2006, Folia Primatologica.

[29]  Yuzhi Cai,et al.  Wild state secrets: ultra‐sensitive measurement of micro‐movement can reveal internal processes in animals , 2014 .

[30]  Athan P. Papailiou,et al.  Behaviors in rhesus monkeys (Macaca mulatta) associated with activity counts measured by accelerometer , 2008, American journal of primatology.

[31]  C. Lowe,et al.  Use of an acceleration data logger to measure diel activity patterns in captive whitetip reef sharks, Triaenodon obesus , 2007 .

[32]  I. Couzin,et al.  Shared decision-making drives collective movement in wild baboons , 2015, Science.

[33]  Robert S Laramee,et al.  Prying into the intimate secrets of animal lives; software beyond hardware for comprehensive annotation in ‘Daily Diary’ tags , 2015, Movement ecology.

[34]  Sergio A. Lambertucci,et al.  Energy Landscapes Shape Animal Movement Ecology , 2013, The American Naturalist.

[35]  Leo Breiman,et al.  Classification and Regression Trees , 1984 .

[36]  Renée Bergeron,et al.  Validation of accelerometers to automatically record sow postures and stepping behaviour , 2010 .

[37]  J. Croxall,et al.  Diving Behavior and Energetics During Foraging Cycles in King Penguins , 1992 .

[38]  T. Guilford,et al.  Migration and stopover in a small pelagic seabird, the Manx shearwater Puffinus puffinus: insights from machine learning , 2009, Proceedings of the Royal Society B: Biological Sciences.

[39]  Rory P. Wilson,et al.  Moving towards acceleration for estimates of activity-specific metabolic rate in free-living animals: the case of the cormorant. , 2006, The Journal of animal ecology.

[40]  William F Fagan,et al.  Transient windows for connectivity in a changing world , 2014, Movement Ecology.

[41]  R. A. Hill,et al.  Human observers impact habituated samango monkeys’ perceived landscape of fear. , 2014 .

[42]  S. Cooke Biotelemetry and biologging in endangered species research and animal conservation: relevance to regional, national, and IUCN Red List threat assessments , 2008 .

[43]  Horst Bornemann,et al.  Fine-scale feeding behavior of Weddell seals revealed by a mandible accelerometer , 2010 .

[44]  Andrew J. King,et al.  A rule-of-thumb based on social affiliation explains collective movements in desert baboons , 2011, Animal Behaviour.

[45]  Orr Spiegel,et al.  AcceleRater: a web application for supervised learning of behavioral modes from acceleration measurements , 2014, Movement ecology.

[46]  J. Fryxell,et al.  Are there general mechanisms of animal home range behaviour? A review and prospects for future research. , 2008, Ecology letters.

[47]  B. Beisner,et al.  Human-wildlife conflict: proximate predictors of aggression between humans and rhesus macaques in India. , 2015, American journal of physical anthropology.

[48]  Yasuhiko Naito,et al.  A new technique for monitoring the detailed behaviour of terrestrial animals: A case study with the domestic cat , 2005 .

[49]  N. Leader‐Williams,et al.  Local attitudes and perceptions toward crop‐raiding by orangutans (Pongo abelii) and other nonhuman primates in northern Sumatra, Indonesia , 2010, American journal of primatology.

[50]  Pascal Monestiez,et al.  Prey capture attempts can be detected in Steller sea lions and other marine predators using accelerometers , 2010, Polar Biology.

[51]  J. Swenson,et al.  An Individual-Based Method to Measure Animal Activity Levels: A Test on Brown Bears , 2006 .

[52]  Richard McFarland,et al.  Assessing the reliability of biologger techniques to measure activity in a free-ranging primate , 2013, Animal Behaviour.

[53]  G. Fehlmann,et al.  Adaptive space use by baboons (Papio ursinus) in response to management interventions in a human‐changed landscape , 2017 .

[54]  Andrew E. Myers,et al.  Derivation of body motion via appropriate smoothing of acceleration data , 2008 .

[55]  P. Hammerstein,et al.  Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism and mating , 1994, Behavioral Ecology and Sociobiology.

[56]  S. Strum The Development of Primate Raiding: Implications for Management and Conservation , 2010, International Journal of Primatology.

[57]  D. Sims,et al.  Minimizing errors in identifying Lévy flight behaviour of organisms. , 2007, The Journal of animal ecology.

[58]  Andreas Buerkert,et al.  Use of a tri-axial accelerometer for automated recording and classification of goats' grazing behaviour , 2009 .

[59]  W. Sellers,et al.  Automatic Monitoring of Primate Locomotor Behaviour Using Accelerometers , 2004, Folia Primatologica.

[60]  M. Kolehmainen,et al.  Cow behaviour pattern recognition using a three-dimensional accelerometer and support vector machines , 2009 .

[61]  I. Boyd,et al.  Bio-logging science: sensing beyond the boundaries , 2004 .