Quantifying Inter- and Intra-Population Niche Variability Using Hierarchical Bayesian Stable Isotope Mixing Models

Variability in resource use defines the width of a trophic niche occupied by a population. Intra-population variability in resource use may occur across hierarchical levels of population structure from individuals to subpopulations. Understanding how levels of population organization contribute to population niche width is critical to ecology and evolution. Here we describe a hierarchical stable isotope mixing model that can simultaneously estimate both the prey composition of a consumer diet and the diet variability among individuals and across levels of population organization. By explicitly estimating variance components for multiple scales, the model can deconstruct the niche width of a consumer population into relevant levels of population structure. We apply this new approach to stable isotope data from a population of gray wolves from coastal British Columbia, and show support for extensive intra-population niche variability among individuals, social groups, and geographically isolated subpopulations. The analytic method we describe improves mixing models by accounting for diet variability, and improves isotope niche width analysis by quantitatively assessing the contribution of levels of organization to the niche width of a population.

[1]  D. Bolnick.  Intraspecific competition favours niche width expansion in Drosophila melanogaster , 2001, Nature.

[2]  Hansen,et al.  Assessing niche differences of sex, armour and asymmetry phenotypes using stable isotope analyses in Haida Gwaii sticklebacks , 2008 .

[3]  C. Darimont,et al.  Stable isotopic niche predicts fitness of prey in a wolf–deer system , 2007 .

[4]  Nathan Wolf,et al.  Isotopic ecology ten years after a call for more laboratory experiments , 2009, Biological reviews of the Cambridge Philosophical Society.

[5]  Márcio S. Araújo,et al.  Using δ13C stable isotopes to quantify individual-level diet variation , 2007, Oecologia.

[6]  T. Caraco,et al.  Social Foraging Theory , 2018 .

[7]  R. Clarke,et al.  Rates of food intake and aggression of oystercatchers Haematopus ostralegus on the most and least preferred mussel Mytilus edulis beds of the exe estuary , 1984 .

[8]  M. Price,et al.  Predators in natural fragments: foraging ecology of wolves in British Columbia's central and north coast archipelago , 2004 .

[9]  G. Polis.  Age Structure Component of Niche Width and Intraspecific Resource Partitioning: Can Age Groups Function as Ecological Species? , 1984, The American Naturalist.

[10]  T. Price.  Diet Variation in a Population of Darwin's Finches , 1987 .

[11]  Lennart Persson,et al.  Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous , 2007, Proceedings of the National Academy of Sciences.

[12]  S. Carleton,et al.  Ten years of experimental animal isotopic ecology , 2009 .

[13]  A. Mazumder,et al.  A critical evaluation of intrapopulation variation of δ13C and isotopic evidence of individual specialization , 2004, Oecologia.

[14]  J. Roughgarden.  Theory of Population Genetics and Evolutionary Ecology: An Introduction , 1995 .

[15]  Robert D. Holt,et al.  Genetic Variation for Habitat Preference: Evidence and Explanations , 1991, The American Naturalist.

[16]  C. Darimont,et al.  Landscape heterogeneity and marine subsidy generate extensive intrapopulation niche diversity in a large terrestrial vertebrate. , 2009, The Journal of animal ecology.

[17]  R. Fuller,et al.  Determining trophic niche width: a novel approach using stable isotope analysis , 2004 .

[18]  J. Thoday,et al.  Evolution of Niche Width , 1974, The American Naturalist.

[19]  D. Phillips,et al.  A niche for isotopic ecology , 2007 .

[20]  Brice X Semmens,et al.  Incorporating uncertainty and prior information into stable isotope mixing models. , 2008, Ecology letters.

[21]  M. A. Leibold.  The Niche Concept Revisited: Mechanistic Models and Community Context , 1995 .

[22]  Daniel I. Bolnick,et al.  MEASURING INDIVIDUAL-LEVEL RESOURCE SPECIALIZATION , 2002 .

[23]  Jacob E. Allgeier,et al.  Niche width collapse in a resilient top predator following ecosystem fragmentation , 2007, Ecology letters.

[24]  S. Shen,et al.  The statistical analysis of compositional data , 1983 .

[25]  L. V. Valen,et al.  MORPHOLOGICAL VARIATION AND WIDTH OF ECOLOGICAL NICHE , 1965 .

[26]  C. Simenstad,et al.  Multi‐source mixing models to quantify food web sources and pathways , 2004 .

[27]  V. Pawlowsky-Glahn,et al.  Simplicial geometry for compositional data , 2006, Geological Society, London, Special Publications.

[28]  John K Kruschke,et al.  Bayesian data analysis. , 2010, Wiley interdisciplinary reviews. Cognitive science.

[29]  Bradley P. Carlin,et al.  Bayesian measures of model complexity and fit , 2002 .

[30]  Louie H. Yang,et al.  The Ecology of Individuals: Incidence and Implications of Individual Specialization , 2002, The American Naturalist.

[31]  Daniel I Bolnick,et al.  Intraspecific competition drives increased resource use diversity within a natural population , 2007, Proceedings of the Royal Society B: Biological Sciences.

[32]  Bruce E. Lyon,et al.  Individual variation in prey selection by sea otters: patterns, causes and implications , 2003 .

[33]  R. Shine.  Ecological Causes for the Evolution of Sexual Dimorphism: A Review of the Evidence , 1989, The Quarterly Review of Biology.

[34]  M. J. Deniro,et al.  Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals , 1984 .

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

[36]  D. Post,et al.  Can stable isotope ratios provide for community-wide measures of trophic structure? , 2007, Ecology.

[37]  H. Berg.  Cold Spring Harbor Symposia on Quantitative Biology.: Vol. LII. Evolution of Catalytic Functions. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 1987, ISBN 0-87969-054-2, xix + 955 pp., US $150.00. , 1989 .

[38]  B. Fry,et al.  Grasshopper Food Web Analysis: Use of Carbon Isotope Ratios to Examine Feeding Relationships Among Terrestrial Herbivores , 1978 .

[39]  Joseph Hilbe,et al.  Data Analysis Using Regression and Multilevel/Hierarchical Models , 2009 .

[40]  E. Angulo,et al.  Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction , 2009 .

[41]  D. Hoeinghaus,et al.  Can stable isotope ratios provide for community-wide measures of trophic structure? , 2007 .

[42]  P. Gustafson,et al.  Conservative prior distributions for variance parameters in hierarchical models , 2006 .

[43]  M. Cadotte.  Ecological Niches: Linking Classical and Contemporary Approaches , 2004, Biodiversity & Conservation.

[44]  Donald L. Phillips,et al.  Uncertainty in source partitioning using stable isotopes , 2017, Oecologia.

[45]  Andrew L Jackson,et al.  Erroneous behaviour of MixSIR, a recently published Bayesian isotope mixing model: a discussion of Moore & Semmens (2008). , 2009, Ecology letters.

[46]  A. Cohen,et al.  Interpreting stable isotopes in food webs: Recognizing the role of time averaging at different trophic levels , 2002 .

[47]  A. Radford,et al.  Bill dimorphism and foraging niche partitioning in the green woodhoopoe , 2003 .

[48]  G. Mateu-Figueras,et al.  Compositional Data Analysis in the Geosciences: From Theory to Practice , 2006 .