Objective classification of latent behavioral states in bio-logging data using multivariate-normal hidden Markov models.

Analysis of complex time-series data from ecological system study requires quantitative tools for objective description and classification. These tools must take into account largely ignored problems of bias in manual classification, autocorrelation, and noise. Here we describe a method using existing estimation techniques for multivariate-normal hidden Markov models (HMMs) to develop such a classification. We use high-resolution behavioral data from bio-loggers attached to free-roaming pelagic tuna as an example. Observed patterns are assumed to be generated by an unseen Markov process that switches between several multivariate-normal distributions. Our approach is assessed in two parts. The first uses simulation experiments, from which the ability of the HMM to estimate known parameter values is examined using artificial time series of data consistent with hypotheses about pelagic predator foraging ecology. The second is the application to time series of continuous vertical movement data from yellowfin and bigeye tuna taken from tuna tagging experiments. These data were compressed into summary metrics capturing the variation of patterns in diving behavior and formed into a multivariate time series used to estimate a HMM. Each observation was associated with covariate information incorporating the effect of day and night on behavioral switching. Known parameter values were well recovered by the HMMs in our simulation experiments, resulting in mean correct classification rates of 90-97%, although some variance-covariance parameters were estimated less accurately. HMMs with two distinct behavioral states were selected for every time series of real tuna data, predicting a shallow warm state, which was similar across all individuals, and a deep colder state, which was more variable. Marked diurnal behavioral switching was predicted, consistent with many previous empirical studies on tuna. HMMs provide easily interpretable models for the objective classification of many different types of noisy autocorrelated data, as typically found across a range of ecological systems. Summarizing time-series data into a multivariate assemblage of dimensions relevant to the desired classification provides a means to examine these data in an appropriate behavioral space. We discuss how outputs of these models can be applied to bio-logging and other imperfect behavioral data, providing easily interpretable models for hypothesis testing.

[1]  Barbara A. Block,et al.  Movements, behavior, and habitat utilization of yellowfin tuna (Thunnus albacares) in the northeastern Pacific Ocean, ascertained through archival tag data , 2007 .

[2]  Geoffrey J. McLachlan,et al.  Robust mixture modelling using the t distribution , 2000, Stat. Comput..

[3]  A. Jassby,et al.  Detecting Changes in Ecological Time Series , 1990 .

[4]  David A. Fournier,et al.  Physiological and behavioural thermoregulation in bigeye tuna (Thunnus obesus) , 1992, Nature.

[5]  John A. Nelder,et al.  A Simplex Method for Function Minimization , 1965, Comput. J..

[6]  Olivier Maury,et al.  An overview of APECOSM, a spatialized mass balanced “Apex Predators ECOSystem Model” to study physiologically structured tuna population dynamics in their ecosystem , 2010 .

[7]  Kurt M. Schaefer,et al.  Vertical movements, behavior, and habitat of bigeye tuna (Thunnus obesus) in the equatorial eastern Pacific Ocean, ascertained from archival tag data , 2010 .

[8]  Erwan Josse,et al.  Tuna food habits related to the micronekton distribution in French Polynesia , 2002 .

[9]  K. M. Schaefer,et al.  Tracking apex marine predator movements in a dynamic ocean , 2011, Nature.

[10]  Mark J. F. Gales,et al.  The Application of Hidden Markov Models in Speech Recognition , 2007, Found. Trends Signal Process..

[11]  Alfred Inselberg,et al.  The plane with parallel coordinates , 1985, The Visual Computer.

[12]  Pasi Fränti,et al.  Knee Point Detection on Bayesian Information Criterion , 2008, 2008 20th IEEE International Conference on Tools with Artificial Intelligence.

[13]  I. Ohta,et al.  Periodic behavior and residence time of yellowfin and bigeye tuna associated with fish aggregating devices around Okinawa Islands, as identified with automated listening stations , 2005 .

[14]  A. Gallagher,et al.  A review of shark satellite tagging studies , 2011 .

[15]  S Schliehe-Diecks,et al.  On the application of mixed hidden Markov models to multiple behavioural time series , 2012, Interface Focus.

[16]  Shingo Kimura,et al.  Vertical behavior of juvenile yellowfin tuna Thunnus albacares in the southwestern part of Japan based on archival tagging , 2013, Fisheries Science.

[17]  Robin Freeman,et al.  Behavioural mapping of a pelagic seabird: combining multiple sensors and a hidden Markov model reveals the distribution of at-sea behaviour , 2013, Journal of The Royal Society Interface.

[18]  Toby A Patterson,et al.  Classifying movement behaviour in relation to environmental conditions using hidden Markov models. , 2009, The Journal of animal ecology.

[19]  Nicolas E. Humphries,et al.  Scaling laws of marine predator search behaviour , 2008, Nature.

[20]  Jean-Louis Deneubourg,et al.  Size-dependent behavior of tuna in an array of fish aggregating devices (FADs) , 2012 .

[21]  David Itano,et al.  Deep diving behavior observed in yellowfin tuna ( Thunnus albacares ) , 2006 .

[22]  Patrick Lehodey,et al.  A spatial ecosystem and populations dynamics model (SEAPODYM) – Modeling of tuna and tuna-like populations , 2008 .

[23]  Henri Weimerskirch,et al.  Top marine predators track Lagrangian coherent structures , 2009, Proceedings of the National Academy of Sciences.

[24]  A. Raftery A model for high-order Markov chains , 1985 .

[25]  S. Campana,et al.  Migration Pathways, Behavioural Thermoregulation and Overwintering Grounds of Blue Sharks in the Northwest Atlantic , 2011, PloS one.

[26]  Scott H. Holan,et al.  Hierarchical Bayesian Markov switching models with application to predicting spawning success of shovelnose sturgeon , 2009 .

[27]  Robert J. Olson,et al.  Apex Predation by Yellowfïn Tuna (Thunnus albacares): Independent Estimates from Gastric Evacuation and Stomach Contents, Bioenergetics, and Cesium Concentrations , 1986 .

[28]  J. M. Cornelius,et al.  Locating Discontinuities along Ecological Gradients , 1987 .

[29]  Kevin Stokes,et al.  Coping with uncertainty in ecological advice: lessons from fisheries , 2003 .

[30]  D P Hartmann,et al.  Interrupted time-series analysis and its application to behavioral data. , 1980, Journal of applied behavior analysis.

[31]  Karen Evans,et al.  Recent advances in bio-logging science: Technologies and methods for understanding animal behaviour and physiology and their environments , 2013 .

[32]  B. Block Physiological Ecology in the 21st Century: Advancements in Biologging Science1 , 2005, Integrative and comparative biology.

[33]  Barbara A. Block,et al.  Habitat use in Atlantic bluefin tuna Thunnus thynnus inferred from diving behavior , 2009 .

[34]  Sabrina Fossette,et al.  Marine animal behaviour: neglecting ocean currents can lead us up the wrong track , 2006, Proceedings of the Royal Society B: Biological Sciences.

[35]  R. A. Leibler,et al.  On Information and Sufficiency , 1951 .

[36]  Tom Hart,et al.  Behavioural switching in a central place forager: patterns of diving behaviour in the macaroni penguin (Eudyptes chrysolophus) , 2010 .

[37]  Henri Weimerskirch,et al.  The importance of oceanographic fronts to marine birds and mammals of the southern oceans , 2009 .

[38]  D. Lindenmayer,et al.  Modelling the abundance of rare species: statistical models for counts with extra zeros , 1996 .

[39]  Nicolas E. Humphries,et al.  Environmental context explains Lévy and Brownian movement patterns of marine predators , 2010, Nature.

[40]  Ian L. Boyd,et al.  THE BEHAVIORAL BASIS FOR NONLINEAR FUNCTIONAL RESPONSES AND OPTIMAL FORAGING IN ANTARCTIC FUR SEALS , 2004 .

[41]  David Sean Kirby,et al.  On the Integrated Study of Tuna Behaviour and Spatial Dynamics: Tagging and Modelling as Complementary Tools , 2001 .

[42]  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.

[43]  Danielle J. Marceau,et al.  The role of agent-based models in wildlife ecology and management , 2011 .

[44]  Wei-Cheng Su,et al.  Vertical and horizontal movements of sailfish (Istiophorus platypterus) near Taiwan determined using pop-up satellite tags , 2011 .

[45]  Shenfeng Fei,et al.  Ecological forecasting and data assimilation in a data-rich era. , 2011, Ecological applications : a publication of the Ecological Society of America.

[46]  Barbara A. Block,et al.  Vertical Movements and Habitat Utilization of Skipjack (Katsuwonus pelamis), Yellowfin (Thunnus albacares), and Bigeye (Thunnus obesus) Tunas in the Equatorial Eastern Pacific Ocean, Ascertained Through Archival Tag Data , 2009 .

[47]  G. Celeux,et al.  An entropy criterion for assessing the number of clusters in a mixture model , 1996 .

[48]  S. Levin The problem of pattern and scale in ecology , 1992 .

[49]  Geoffrey J. McLachlan,et al.  Finite Mixture Models , 2019, Annual Review of Statistics and Its Application.

[50]  David W. Sims,et al.  Satellite tracking of the World's largest bony fish, the ocean sunfish (Mola mola L.) in the North East Atlantic , 2009 .

[51]  Richard W. Brill,et al.  Vertical movements of bigeye tuna (Thunnus obesus) associated with islands, buoys, and seamounts near the main Hawaiian Islands from archival tagging data , 2003 .

[52]  L. M. Berliner,et al.  A Bayesian tutorial for data assimilation , 2007 .

[53]  J. A. Hartigan,et al.  A k-means clustering algorithm , 1979 .

[54]  C. Phillip Goodyear,et al.  Hypoxia-based habitat compression of tropical pelagic fishes , 2006 .

[55]  Stephen P. Ellner,et al.  SCALING UP ANIMAL MOVEMENTS IN HETEROGENEOUS LANDSCAPES: THE IMPORTANCE OF BEHAVIOR , 2002 .

[56]  Gene R. Ploskey,et al.  The Juvenile Salmon Acoustic Telemetry System: A New Tool , 2010 .

[57]  David M. Forsyth,et al.  Exploitation ecosystems and trophic cascades in non-equilibrium systems: pasture – red kangaroo – dingo interactions in arid Australia , 2013 .

[58]  F. Menczer,et al.  Co-evolution of movement behaviours by tropical pelagic predatory fishes in response to prey environment: a simulation model , 2000 .

[59]  T. Lenton Early warning of climate tipping points , 2011 .

[60]  M. Musyl,et al.  Differential heating and cooling rates in bigeye tuna (Thunnus obesus Lowe): a model of non-steady state heat exchange , 2007, Journal of Experimental Biology.

[61]  Kim N. Holland,et al.  A rapid ontogenetic shift in the diet of juvenile yellowfin tuna from Hawaii , 2006 .

[62]  Elliott L. Hazen,et al.  The Relationship among Oceanography, Prey Fields, and Beaked Whale Foraging Habitat in the Tongue of the Ocean , 2011, PloS one.