Using partially specified models to detect and quantify structural sensitivity in biological systems

Mathematical models in ecology and evolution are highly simplified representations of a complex underlying reality. For this reason, there is always a high degree of uncertainty with regards to the model specification—not just in terms of parameters, but also in the form taken by the model equations themselves. This uncertainty becomes critical for models in which the use of two different functions fitting the same dataset can yield substantially different model predictions—a property known as structural sensitivity. In this case, even if the model is purely deterministic, the uncertainty in the model functions carries through into uncertainty in the model predictions, and new frameworks are required to tackle this fundamental problem. Here, we construct a framework that uses partially specified models: ODE models in which unknown functions are represented not by a specific functional form, but by an entire data range and constraints of biological realism. Partially specified models can be used to rigorously detect when models are structurally sensitive in their predictions concerning the character of an equilibrium point by projecting the data range into a generalised bifurcation space formed of equilibrium values and derivatives of any unspecified functions. The key question of how to carry out this projection is a serious mathematical challenge and an obstacle to the use of partially specified models. We address this challenge by developing several powerful techniques to perform such a projection.

[1]  C. S. Holling The functional response of invertebrate predators to prey density , 1966 .

[2]  J. Steele,et al.  The role of predation in plankton models , 1992 .

[3]  B. Quéguiner,et al.  How far details are important in ecosystem modelling: the case of multi-limiting nutrients in phytoplankton–zooplankton interactions , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[4]  Simon N. Wood,et al.  PARTIALLY SPECIFIED ECOLOGICAL MODELS , 2001 .

[5]  M. Duffy,et al.  Rapid evolution and ecological host-parasite dynamics. , 2007, Ecology letters.

[6]  M A Lewis,et al.  How predation can slow, stop or reverse a prey invasion , 2001, Bulletin of mathematical biology.

[7]  R. Arditi,et al.  Variation in Plankton Densities Among Lakes: A Case for Ratio-Dependent Predation Models , 1991, The American Naturalist.

[8]  John D. Reeve,et al.  Predation and bark beetle dynamics , 1997, Oecologia.

[9]  A. M. Edwards,et al.  The invisible niche: weakly density-dependent mortality and the coexistence of species. , 2009, Journal of theoretical biology.

[10]  M. Rosenzweig Paradox of Enrichment: Destabilization of Exploitation Ecosystems in Ecological Time , 1971, Science.

[11]  Michio Kondoh,et al.  Response to Comment on "Foraging Adaptation and the Relationship Between Food-Web Complexity and Stability" , 2003, Science.

[12]  H. I. Freedman,et al.  Persistence in predator-prey systems with ratio-dependent predator influence , 1993 .

[13]  M. W. Adamson,et al.  When can we trust our model predictions? Unearthing structural sensitivity in biological systems , 2013, Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[14]  G. Butler,et al.  Predator-mediated competition in the chemostat , 1986 .

[15]  Predator-prey models in heterogeneous environment: Emergence of functional response , 1998 .

[16]  E. Voit,et al.  Recasting nonlinear differential equations as S-systems: a canonical nonlinear form , 1987 .

[17]  Brendan P. Kelaher,et al.  Ratio-dependent response of a temperate Australian estuarine system to sustained nitrogen loading , 2006, Oecologia.

[18]  William A. Nelson,et al.  CAPTURING DYNAMICS WITH THE CORRECT RATES: INVERSE PROBLEMS USING SEMIPARAMETRIC APPROACHES , 2004 .

[19]  David A. Vasseur Populations embedded in trophic communities respond differently to coloured environmental noise. , 2007, Theoretical population biology.

[20]  S. Levin,et al.  OSCILLATORY DYNAMICS AND SPATIAL SCALE: THE ROLE OF NOISE AND UNRESOLVED PATTERN , 2001 .

[21]  R. Arditi,et al.  Coupling in predator-prey dynamics: Ratio-Dependence , 1989 .

[22]  Trevor Platt,et al.  Mathematical formulation of the relationship between photosynthesis and light for phytoplankton , 1976 .

[23]  Marten Scheffer,et al.  Resonance of Plankton Communities with Temperature Fluctuations , 2011, The American Naturalist.

[24]  A. Morozov Incorporating Complex Foraging of Zooplankton in Models: Role of Micro- and Mesoscale Processes in Macroscale Patterns , 2013 .

[25]  Malay Banerjee,et al.  Bifurcation analysis of a ratio-dependent prey-predator model with the Allee effect , 2012 .

[26]  James W. Murray,et al.  Functional responses for zooplankton feeding on multiple resources: a review of assumptions and biological dynamics , 2003 .

[27]  D. DeAngelis,et al.  Effects of spatial grouping on the functional response of predators. , 1999, Theoretical population biology.

[28]  Jonathan M. Jeschke,et al.  PREDATOR FUNCTIONAL RESPONSES: DISCRIMINATING BETWEEN HANDLING AND DIGESTING PREY , 2002 .

[29]  R. P. Canale,et al.  Experimental and mathematical modeling studies of protozoan predation on bacteria , 1973 .

[30]  P. Auger,et al.  Study of a virus–bacteria interaction model in a chemostat: application of geometrical singular perturbation theory , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[31]  James H. Brown,et al.  Long-term dynamics of winter and summer annual communities in the Chihuahuan Desert , 2002 .

[32]  W. R. Demott,et al.  Feeding selectivities and relative ingestion rates of Daphnia and Bosmina1 , 1982 .

[33]  C. Philippart,et al.  Long‐term phytoplankton‐nutrient interactions in a shallow coastal sea: Algal community structure, nutrient budgets, and denitrification potential , 2000 .

[34]  S. Ellner,et al.  Testing for predator dependence in predator-prey dynamics: a non-parametric approach , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[35]  J. Truscott,et al.  Equilibria, stability and excitability in a general class of plankton population models , 1994, Philosophical Transactions of the Royal Society of London. Series A: Physical and Engineering Sciences.

[36]  R. Sanders,et al.  UNCSAM: a tool for automating sensitivity and uncertainty analysis , 1994 .

[37]  Jim M Cushing,et al.  ESTIMATING CHAOS AND COMPLEX DYNAMICS IN AN INSECT POPULATION , 2001 .

[38]  J. Dieudonne Foundations of Modern Analysis , 1969 .

[39]  A. Morozov,et al.  Emergence of Holling type III zooplankton functional response: bringing together field evidence and mathematical modelling. , 2010, Journal of theoretical biology.

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

[41]  Brian D. Fath,et al.  Fundamentals of Ecological Modelling: Applications in Environmental Management and Research , 2011 .

[42]  S. Hsu,et al.  Global analysis of the Michaelis–Menten-type ratio-dependent predator-prey system , 2001, Journal of mathematical biology.

[43]  Andrew M. Edwards,et al.  Adding Detritus to a Nutrient–Phytoplankton–Zooplankton Model:A Dynamical-Systems Approach , 2001 .

[44]  Yang Kuang,et al.  Global qualitative analysis of a ratio-dependent predator–prey system , 1998 .

[45]  I. Chou,et al.  Recent developments in parameter estimation and structure identification of biochemical and genomic systems. , 2009, Mathematical biosciences.

[46]  M. W. Adamson,et al.  Bifurcation Analysis of Models with Uncertain Function Specification: How Should We Proceed? , 2014, Bulletin of mathematical biology.

[47]  R. Macarthur,et al.  Graphical Representation and Stability Conditions of Predator-Prey Interactions , 1963, The American Naturalist.

[48]  Ludek Berec,et al.  Multiple Allee effects and population management. , 2007, Trends in ecology & evolution.

[49]  T. Smayda Patterns of variability characterizing marine phytoplankton, with examples from Narragansett Bay , 1998 .

[50]  Thilo Gross,et al.  Dynamical analysis of evolution equations in generalized models , 2010, 1012.4340.

[51]  M. Kinnison,et al.  Eco-evolutionary conservation biology: contemporary evolution and the dynamics of persistence , 2007 .

[52]  M. Kot,et al.  Speeds of invasion in a model with strong or weak Allee effects. , 2001, Mathematical biosciences.

[53]  M. W. Adamson,et al.  Evolution of virulence driven by predator-prey interaction: Possible consequences for population dynamics. , 2011, Journal of theoretical biology.

[54]  Andrew Morozov,et al.  Structural sensitivity of biological models revisited. , 2011, Journal of theoretical biology.

[55]  William W. Murdoch,et al.  Functional Response and Stability in Predator-Prey Systems , 1975, The American Naturalist.

[56]  Francis J Doyle,et al.  Dynamic energy budgets in syntrophic symbiotic relationships between heterotrophic hosts and photoautotrophic symbionts. , 2009, Journal of theoretical biology.

[57]  R. Arditi,et al.  Empirical Evidence of the Role of Heterogeneity in Ratio‐Dependent Consumption , 1993 .

[58]  William F. Morris,et al.  PROBLEMS IN DETECTING CHAOTIC BEHAVIOR IN NATURAL POPULATIONS BY FITTING SIMPLE DISCRETE MODELS , 1990 .

[59]  K. Tande,et al.  On the trophic fate of Phaeocystis pouchetii (Harlot). III. Functional responses in grazing demonstrated on juvenile stages of Calanus finmarchicus (Copepoda) fed diatoms and Phaeocystis , 1990 .

[60]  Global dynamics and bifurcation of a tri-trophic food chain model , 2010 .

[61]  Thilo Gross,et al.  Structural kinetic modeling of metabolic networks , 2006, Proceedings of the National Academy of Sciences.

[62]  Bernd Blasius,et al.  Community response to enrichment is highly sensitive to model structure , 2005, Biology Letters.

[63]  H. J. Gold,et al.  A Monte Carlo/response surface strategy for sensitivity analysis: application to a dynamic model of vegetative plant growth. , 1989, Applied mathematical modelling.

[64]  Ulf Dieckmann,et al.  Trade‐Off Geometries and Frequency‐Dependent Selection , 2004, The American Naturalist.

[65]  S. Falk‐Petersen,et al.  Influence of spatial heterogeneity on the type of zooplankton functional response: A study based on field observations , 2008 .

[66]  Hopf bifurcation in pioneer-climax competing species models. , 1996, Mathematical biosciences.

[67]  M E Gilpin,et al.  Enriched predator-prey systems: theoretical stability. , 1972, Science.

[68]  Mary R. Myerscough,et al.  Stability, persistence and structural stability in a classical predator-prey model , 1996 .

[69]  Robert P Freckleton,et al.  Census error and the detection of density dependence. , 2006, The Journal of animal ecology.

[70]  Thilo Gross,et al.  Enrichment and foodchain stability: the impact of different forms of predator-prey interaction. , 2004, Journal of theoretical biology.

[71]  Frederic A. Hopf,et al.  The role of the Allee effect in species packing , 1985 .

[72]  R Arditi,et al.  Parametric analysis of the ratio-dependent predator–prey model , 2001, Journal of mathematical biology.

[73]  J. Douglas Faires,et al.  Numerical Analysis , 1981 .

[74]  Thomas R. Anderson,et al.  Influence of grazing formulations on the emergent properties of a complex ecosystem model in a global ocean general circulation model , 2010 .

[75]  Christian Jost,et al.  About deterministic extinction in ratio-dependent predator-prey models , 1999 .

[76]  T. Benton,et al.  The Amplification of Environmental Noise in Population Models: Causes and Consequences , 2003, The American Naturalist.

[77]  S. Wood,et al.  Estimation of Mortality Rates in Stage-Structured Population , 1991 .

[78]  J. N. Thompson,et al.  Rapid evolution as an ecological process. , 1998, Trends in ecology & evolution.

[79]  R. Tischner,et al.  Nitrate uptake and nitrate reduction in synchronous Chlorella , 2004, Planta.

[80]  M. Llope,et al.  A decade of sampling in the Bay of Biscay: What are the zooplankton time series telling us? , 2007 .

[81]  J. A.,et al.  The Self-Adjustment of Populations to Change , 2008 .

[82]  Quantifying uncertainty in partially specified biological models: how can optimal control theory help us? , 2016, Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[83]  L. Ginzburg,et al.  The nature of predation: prey dependent, ratio dependent or neither? , 2000, Trends in ecology & evolution.

[84]  P. Giller,et al.  Spatial and temporal co-occurrence of competitors in Southern african dung beetle communities , 1994 .

[85]  G. F. Gause,et al.  EXPERIMENTAL ANALYSIS OF VITO VOLTERRA'S MATHEMATICAL THEORY OF THE STRUGGLE FOR EXISTENCE. , 1934, Science.

[86]  Horst Malchow,et al.  Experimental demonstration of chaos in a microbial food web , 2005, Nature.

[87]  R. Arditi,et al.  Emergence of donor control in patchy predator—prey systems , 1998 .

[88]  H. Wolda Insect Seasonality: Why? , 1988 .

[89]  M. Andrew,et al.  Structural sensitivity of biological models revisited. , 2011 .

[90]  Y. Kuznetsov Elements of Applied Bifurcation Theory , 2023, Applied Mathematical Sciences.

[91]  P. Kareiva,et al.  Allee Dynamics and the Spread of Invading Organisms , 1993 .

[92]  M. W. Adamson,et al.  Defining and detecting structural sensitivity in biological models: developing a new framework , 2014, Journal of mathematical biology.

[93]  M. W. Adamson,et al.  Revising the Role of Species Mobility in Maintaining Biodiversity in Communities with Cyclic Competition , 2012, Bulletin of Mathematical Biology.

[94]  Eduardo González-Olivares,et al.  Dynamical complexities in the Leslie–Gower predator–prey model as consequences of the Allee effect on prey , 2011 .

[95]  Stephen P. Ellner,et al.  Living on the edge of chaos: population dynamics of fennoscandian voles , 2000 .

[96]  Yang Kuang,et al.  Uniqueness of limit cycles in Gause-type models of predator-prey systems , 1988 .

[97]  S. Ellner,et al.  Rapid contemporary evolution and clonal food web dynamics , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[98]  William Gurney,et al.  FORMULATING AND TESTING A PARTIALLY SPECIFIED DYNAMIC ENERGY BUDGET MODEL , 2004 .

[99]  Simon N. Wood,et al.  Super–sensitivity to structure in biological models , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[100]  É. Kisdi,et al.  Evolution of pathogen virulence under selective predation: a construction method to find eco-evolutionary cycles. , 2013, Journal of theoretical biology.

[101]  Mark Pagel,et al.  On the Regulation of Populations of Mammals, Birds, Fish, and Insects , 2005, Science.

[102]  Eduardo González-Olivares,et al.  Consequences of double Allee effect on the number of limit cycles in a predator-prey model , 2011, Comput. Math. Appl..

[103]  M. Haque,et al.  Ratio-Dependent Predator-Prey Models of Interacting Populations , 2009, Bulletin of mathematical biology.

[104]  S. Kooijman,et al.  Consumption and release of dissolved organic carbon by marine bacteria in a pulsed-substrate environment : from experiments to modelling , 2009 .

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

[106]  S. Chow,et al.  Normal Forms and Bifurcation of Planar Vector Fields , 1994 .

[107]  S. Ellner,et al.  Rapid evolution drives ecological dynamics in a predator–prey system , 2003, Nature.

[108]  Yang Kuang,et al.  Heteroclinic Bifurcation in the Michaelis-Menten-Type Ratio-Dependent Predator-Prey System , 2007, SIAM J. Appl. Math..

[109]  M. Gilpin,et al.  Global models of growth and competition. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[110]  R. Sarkar,et al.  Impacts of Incubation Delay on the Dynamics of an Eco-Epidemiological System—A Theoretical Study , 2008, Bulletin of mathematical biology.

[111]  Dongmei Xiao,et al.  Global dynamics of a ratio-dependent predator-prey system , 2001, Journal of mathematical biology.

[112]  Göran Englund,et al.  Scaling up the functional response for spatially heterogeneous systems. , 2008, Ecology letters.

[113]  Thilo Gross,et al.  Generalized models as a universal approach to the analysis of nonlinear dynamical systems. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[114]  S. Ellner,et al.  Chaos in Ecology: Is Mother Nature a Strange Attractor?* , 1993 .