Estimating parameters from multiple time series of population dynamics using Bayesian inference

Empirical time series of interacting entities, e.g. species abundances, are highly useful to study ecological mechanisms. Mathematical models are valuable tools to further elucidate those mechanisms and underlying processes. However, obtaining an agreement between model predictions and experimental observations remains a demanding task. As models always abstract from reality one parameter often summarizes several properties. Parameter measurements are performed in additional experiments independent of the ones delivering the time series. Transferring these parameter values to different settings may result in incorrect parametrizations. On top of that, the properties of organisms and thus the respective parameter values may vary considerably. These issues limit the use of a priori model parametrizations. In this study, we present a method suited for a direct estimation of model parameters and their variability from experimental time series data. We combine numerical simulations of a continuous-time dynamical population model with Bayesian inference, using a hierarchical framework that allows for variability of individual parameters. The method is applied to a comprehensive set of time series from a laboratory predator-prey system that features both steady states and cyclic population dynamics. Our model predictions are able to reproduce both steady states and cyclic dynamics of the data. Additionally to the direct estimates of the parameter values, the Bayesian approach also provides their uncertainties. We found that fitting cyclic population dynamics, which contain more information on the process rates than steady states, yields more precise parameter estimates. We detected significant variability among parameters of different time series and identified the variation in the maximum growth rate of the prey as a source for the transition from steady states to cyclic dynamics. By lending more flexibility to the model, our approach facilitates parametrizations and shows more easily which patterns in time series can be explained also by simple models. Applying Bayesian inference and dynamical population models in conjunction may help to quantify the profound variability in organismal properties in nature.

[1]  L. Becks,et al.  Different types of synchrony in chaotic and cyclic communities , 2013, Nature Communications.

[2]  Takuo Nagaike,et al.  Estimation of deer population dynamics using a bayesian state‐space model with multiple abundance indices , 2013 .

[3]  Benjamin Rosenbaum,et al.  Fitting functional responses: Direct parameter estimation by simulating differential equations , 2017, bioRxiv.

[4]  Ralph Tiedemann,et al.  Differential response to heat stress among evolutionary lineages of an aquatic invertebrate species complex , 2018, Biology Letters.

[5]  Ruchi M. Newman,et al.  TRIM5 Suppresses Cross-Species Transmission of a Primate Immunodeficiency Virus and Selects for Emergence of Resistant Variants in the New Species , 2010, PLoS biology.

[6]  S. Schreiber,et al.  Why intraspecific trait variation matters in community ecology. , 2011, Trends in ecology & evolution.

[7]  A. Novick,et al.  Description of the chemostat. , 1950, Science.

[8]  G. Bell,et al.  Evolutionary rescue can prevent extinction following environmental change. , 2009, Ecology letters.

[9]  Thomas Hickler,et al.  Long‐term population dynamics of a migrant bird suggests interaction of climate change and competition with resident species , 2015 .

[10]  Olivier Gimenez,et al.  Disentangling the effects of climate, density dependence, and harvest on an iconic large herbivore's population dynamics. , 2015, Ecological applications : a publication of the Ecological Society of America.

[11]  Conor P. McGowan,et al.  Disentangling density‐dependent dynamics using full annual cycle models and Bayesian model weight updating , 2017 .

[12]  Vassily Lyutsarev,et al.  Inferred support for disturbance-recovery hypothesis of North Atlantic phytoplankton blooms , 2015 .

[13]  Philipp H. Boersch-Supan,et al.  deBInfer: Bayesian inference for dynamical models of biological systems in R , 2016, Methods in Ecology and Evolution.

[14]  Jiguo Cao,et al.  Estimating a Predator‐Prey Dynamical Model with the Parameter Cascades Method , 2008, Biometrics.

[15]  Mattias Jonsson,et al.  Ecosystem function in predator–prey food webs—confronting dynamic models with empirical data , 2018, The Journal of animal ecology.

[16]  Guntram Weithoff,et al.  High local trait variability in a globally invasive cyanobacterium , 2017 .

[17]  S. T. Buckland,et al.  Long-term datasets in biodiversity research and monitoring: assessing change in ecological communities through time. , 2010, Trends in ecology & evolution.

[18]  Aki Vehtari,et al.  Limitations of “Limitations of Bayesian Leave-one-out Cross-Validation for Model Selection” , 2018, Computational Brain & Behavior.

[19]  David Welch,et al.  Approximate Bayesian computation scheme for parameter inference and model selection in dynamical systems , 2009, Journal of The Royal Society Interface.

[20]  Peter A. Abrams,et al.  IS PREDATOR‐MEDIATED COEXISTENCE POSSIBLE INUNSTABLE SYSTEMS? , 1999 .

[21]  Cyrille Violle,et al.  The return of the variance: intraspecific variability in community ecology. , 2012, Trends in ecology & evolution.

[22]  Wei Zhang,et al.  Reverse taxonomy applied to the Brachionus calyciflorus cryptic species complex: Morphometric analysis confirms species delimitations revealed by molecular phylogenetic analysis and allows the (re)description of four species , 2018, PloS one.

[23]  S. Ellner,et al.  Crossing the hopf bifurcation in a live predator-prey system. , 2000, Science.

[24]  Brad M. Ochocki,et al.  The effect of demographic correlations on the stochastic population dynamics of perennial plants , 2016 .

[25]  Martyn Plummer,et al.  JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling , 2003 .

[26]  Karen C. Abbott,et al.  Moving forward in circles: challenges and opportunities in modelling population cycles. , 2017, Ecology letters.

[27]  Ricardo Anadón,et al.  Determining the causes behind the collapse of a small pelagic fishery using Bayesian population modeling. , 2015, Ecological applications : a publication of the Ecological Society of America.

[28]  Javier Bustamante,et al.  Estimating partial observability and nonlinear climate effects on stochastic community dynamics of migratory waterfowl. , 2012, The Journal of animal ecology.

[29]  Marc Mangel,et al.  Overcoming the Data Crisis in Biodiversity Conservation. , 2018, Trends in ecology & evolution.

[30]  Boris Worm,et al.  Ecosystem recovery after climatic extremes enhanced by genotypic diversity. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Ursula Gaedke,et al.  High food quality of prey lowers its risk of extinction , 2017 .

[32]  Stephen P Ellner,et al.  Reduction of adaptive genetic diversity radically alters eco-evolutionary community dynamics. , 2010, Ecology letters.

[33]  Erin E. Blankenship,et al.  Fitting population growth models in the presence of measurement and detection error , 2013 .

[34]  Stephen P Ellner,et al.  The functional genomics of an eco-evolutionary feedback loop: linking gene expression, trait evolution, and community dynamics. , 2012, Ecology letters.

[35]  Jim M Cushing,et al.  Nonlinear Stochastic Population Dynamics: The Flour Beetle Tribolium as an Effective Tool of Discovery , 2005 .

[36]  B. Enquist,et al.  Rebuilding community ecology from functional traits. , 2006, Trends in ecology & evolution.

[37]  Gareth W. Peters,et al.  Estimating density dependence and latent population trajectories with unknown observation error , 2012 .

[38]  Michael H. Cortez Genetic variation determines which feedbacks drive and alter predator–prey eco‐evolutionary cycles , 2018 .

[39]  Eric P Palkovacs,et al.  Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[40]  Leslie A. Real,et al.  The Kinetics of Functional Response , 1977, The American Naturalist.

[41]  Ursula Gaedke,et al.  Analyzing the shape of observed trait distributions enables a data‐based moment closure of aggregate models , 2017 .

[42]  Elena Litchman,et al.  Trait-Based Community Ecology of Phytoplankton , 2008 .

[43]  D. Oro,et al.  Size-mediated non-trophic interactions and stochastic predation drive assembly and dynamics in a seabird community. , 2011, Ecology.

[44]  Benjamin M. Bolker,et al.  Ecological Models and Data in R , 2008 .

[45]  Andrew Thomas,et al.  The BUGS project: Evolution, critique and future directions , 2009, Statistics in medicine.

[46]  U. Brose,et al.  Interactive effects of shifting body size and feeding adaptation drive interaction strengths of protist predators under warming , 2017, bioRxiv.

[47]  Ursula Gaedke,et al.  Trait-fitness relationships determine how trade-off shapes affect species coexistence. , 2017, Ecology.

[48]  R. Lande,et al.  Adaptation, Plasticity, and Extinction in a Changing Environment: Towards a Predictive Theory , 2010, PLoS biology.

[49]  Ursula Gaedke,et al.  Accounting for activity respiration results in realistic trophic transfer efficiencies in allometric trophic network (ATN) models , 2018, Theoretical Ecology.

[50]  F. Ruggeri,et al.  Bayesian Inference for Functional Response in a Stochastic Predator–Prey System , 2008, Bulletin of mathematical biology.

[51]  T. Kypraios,et al.  Bayesian inference and model choice for Holling’s disc equation: a case study on an insect predator-prey system , 2016 .

[52]  Ursula Gaedke,et al.  Benchmarking Successional Progress in a Quantitative Food Web , 2014, PloS one.

[53]  F. De Filippis,et al.  A Selected Core Microbiome Drives the Early Stages of Three Popular Italian Cheese Manufactures , 2014, PloS one.

[54]  Neo D. Martinez,et al.  Mechanistic theory and modelling of complex food-web dynamics in Lake Constance. , 2012, Ecology letters.

[55]  James T. Thorson,et al.  Faster estimation of Bayesian models in ecology using Hamiltonian Monte Carlo , 2017 .

[56]  John P. DeLong,et al.  Predator–prey dynamics and the plasticity of predator body size , 2014 .

[57]  Helmut Hillebrand,et al.  Biodiversity in a complex world: consolidation and progress in functional biodiversity research. , 2009, Ecology letters.

[58]  Clifford H. Thurber,et al.  Parameter estimation and inverse problems , 2005 .

[59]  Ursula Gaedke,et al.  Regulation of planktonic ciliate dynamics and functional composition during spring in Lake Constance , 2007 .

[60]  Björn C. Rall,et al.  Analyzing pathogen suppressiveness in bioassays with natural soils using integrative maximum likelihood methods in R , 2016, PeerJ.

[61]  Leah R. Johnson,et al.  Bayesian inference for bioenergetic models , 2013 .

[62]  E. Schulze,et al.  The Jena Experiment: six years of data from a grassland biodiversity experiment , 2010 .