Metapopulation stability in branching river networks

Significance Metapopulation stability is a critical ecological property. Although ecosystem size has been considered as a fundamental driver of metapopulation stability, current theories developed in simplified landscapes may not be appropriate for complex branching ecosystems, such as rivers. Here, we show that a scale-independent characteristic of fractal river networks, branching complexity (measured as branching probability), stabilizes watershed metapopulations. We theoretically revealed that a strong association between branching complexity and metapopulation stability is a consequence of purely probabilistic processes. Furthermore, the stabilizing effect of branching complexity was consistently observed in metapopulations of four ecologically distinct riverine fishes. Hence, branching complexity may be a ubiquitous agent of metapopulation stability in branching ecosystems. The loss of such complexity may undermine resilience of metapopulations. Intraspecific population diversity (specifically, spatial asynchrony of population dynamics) is an essential component of metapopulation stability and persistence in nature. In 2D systems, theory predicts that metapopulation stability should increase with ecosystem size (or habitat network size): Larger ecosystems will harbor more diverse subpopulations with more stable aggregate dynamics. However, current theories developed in simplified landscapes may be inadequate to predict emergent properties of branching ecosystems, an overlooked but widespread habitat geometry. Here, we combine theory and analyses of a unique long-term dataset to show that a scale-invariant characteristic of fractal river networks, branching complexity (measured as branching probability), stabilizes watershed metapopulations. In riverine systems, each branch (i.e., tributary) exhibits distinctive ecological dynamics, and confluences serve as “merging” points of those branches. Hence, increased levels of branching complexity should confer a greater likelihood of integrating asynchronous dynamics over the landscape. We theoretically revealed that the stabilizing effect of branching complexity is a consequence of purely probabilistic processes in natural conditions, where within-branch synchrony exceeds among-branch synchrony. Contrary to current theories developed in 2D systems, metapopulation size (a variable closely related to ecosystem size) had vague effects on metapopulation stability. These theoretical predictions were supported by 18-y observations of fish populations across 31 watersheds: Our cross-watershed comparisons revealed consistent stabilizing effects of branching complexity on metapopulations of very different riverine fishes. A strong association between branching complexity and metapopulation stability is likely to be a pervasive feature of branching networks that strongly affects species persistence during rapid environmental changes.

[1]  Enrico Bertuzzo,et al.  Metapopulation persistence and species spread in river networks. , 2014, Ecology letters.

[2]  W. Fagan,et al.  Living in the branches: population dynamics and ecological processes in dendritic networks. , 2007, Ecology letters.

[3]  D. Lytle,et al.  Adaptation to natural flow regimes. , 2004, Trends in ecology & evolution.

[4]  G. Pess,et al.  Association between geomorphic attributes of watersheds, water temperature, and salmon spawn timing in Alaskan streams , 2013 .

[5]  Matthew J. Denwood,et al.  runjags: An R Package Providing Interface Utilities, Model Templates, Parallel Computing Methods and Additional Distributions for MCMC Models in JAGS , 2016 .

[6]  D. Schindler,et al.  Spawning salmon and the phenology of emergence in stream insects , 2010, Proceedings of the Royal Society B: Biological Sciences.

[7]  Daniel E. Schindler,et al.  The portfolio concept in ecology and evolution , 2015 .

[8]  Yolanda F. Wiersma,et al.  A new measure of longitudinal connectivity for stream networks , 2008, Landscape Ecology.

[9]  Michael Schaub,et al.  Bayesian Population Analysis using WinBUGS: A Hierarchical Perspective , 2011 .

[10]  E. C. Campbell Grant Structural complexity, movement bias, and metapopulation extinction risk in dendritic ecological networks , 2011, Journal of the North American Benthological Society.

[11]  M. Gilpin,et al.  Metapopulation dynamics: a brief his-tory and conceptual domain , 1991 .

[12]  Taku Kadoya,et al.  Trends and stability of inland fishery resources in Japanese lakes: introduction of exotic piscivores as a driver. , 2014, Ecological applications : a publication of the Ecological Society of America.

[13]  Emanuel A. Fronhofer,et al.  Classical metapopulation dynamics and eco‐evolutionary feedbacks in dendritic networks , 2017 .

[14]  D. Doak,et al.  The Statistical Inevitability of Stability‐Diversity Relationships in Community Ecology , 1998, The American Naturalist.

[15]  Gregory D. Williams,et al.  Forty years of seagrass population stability and resilience in an urbanizing estuary , 2017 .

[16]  Jonathan B. Armstrong,et al.  Performance of salmon fishery portfolios across western North America , 2014, The Journal of applied ecology.

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

[18]  J. Olden,et al.  The role of dispersal in river network metacommunities: Patterns, processes, and pathways , 2018 .

[19]  Frederick J. Swanson,et al.  Disturbance regimes of stream and riparian systems — a disturbance‐cascade perspective , 2000 .

[20]  I. Washitani,et al.  Asymmetric dispersal structures a riverine metapopulation of the freshwater pearl mussel Margaritifera laevis , 2014, Ecology and evolution.

[21]  E. Grant Structural complexity, movement bias, and metapopulation extinction risk in dendritic ecological networks , 2011 .

[22]  Florian Altermatt,et al.  Diversity in riverine metacommunities: a network perspective , 2013, Aquatic Ecology.

[23]  N. Dulvy,et al.  Portfolio conservation of metapopulations under climate change. , 2015, Ecological applications : a publication of the Ecological Society of America.

[24]  M. Loreau,et al.  The relationship between the spatial scaling of biodiversity and ecosystem stability. , 2018, Global ecology and biogeography : a journal of macroecology.

[25]  Stream Ecology: Structure and Function of Running Waters , 1994 .

[26]  Daniel E. Schindler,et al.  Synchronization and portfolio performance of threatened salmon , 2010 .

[27]  Emanuel A. Fronhofer,et al.  SPATIALLY CORRELATED EXTINCTIONS SELECT FOR LESS EMIGRATION BUT LARGER DISPERSAL DISTANCES IN THE SPIDER MITE TETRANYCHUS URTICAE , 2014, Evolution; international journal of organic evolution.

[28]  A. Rinaldo,et al.  Dendritic connectivity controls biodiversity patterns in experimental metacommunities , 2012, Proceedings of the National Academy of Sciences.

[29]  M. Chadwick Stream Ecology: Structure and Function of Running Waters , 2008 .

[30]  Sutirth Dey,et al.  Stability via Asynchrony in Drosophila Metapopulations with Low Migration Rates , 2006, Science.

[31]  Lars Y. Pomara,et al.  Climate variability drives population cycling and synchrony , 2017 .

[32]  A. Rinaldo,et al.  Fractal River Basins: Chance and Self-Organization , 1997 .

[33]  J. Finlay,et al.  Stream size and human influences on ecosystem production in river networks , 2011 .

[34]  R. Sparks,et al.  THE NATURAL FLOW REGIME. A PARADIGM FOR RIVER CONSERVATION AND RESTORATION , 1997 .

[35]  Daniel E. Schindler,et al.  Asynchrony in population dynamics of sockeye salmon in southwest Alaska , 2008 .

[36]  D. Post,et al.  ECOSYSTEM SIZE, BUT NOT DISTURBANCE, DETERMINES FOOD-CHAIN LENGTH ON ISLANDS OF THE BAHAMAS. , 2008, Ecology.

[37]  M. Loreau,et al.  Dispersal and metapopulation stability , 2015, PeerJ.

[38]  T. Quinn,et al.  A metapopulation perspective for salmon and other anadromous fish , 2007 .

[39]  G. Likens,et al.  Stable isotopes identify dispersal patterns of stonefly populations living along stream corridors , 2005 .

[40]  Andrea Rinaldo,et al.  Complex Interaction of Dendritic Connectivity and Hierarchical Patch Size on Biodiversity in River-Like Landscapes , 2013, The American Naturalist.

[41]  A. Rinaldo,et al.  River networks as ecological corridors: A coherent ecohydrological perspective , 2018, Advances in water resources.

[42]  C. Swan,et al.  Dendritic network structure constrains metacommunity properties in riverine ecosystems. , 2010, The Journal of animal ecology.

[43]  Marc Kéry Chapter 3 – WinBUGS , 2010 .

[44]  David J. Lunn,et al.  The BUGS Book: A Practical Introduction to Bayesian Analysis , 2013 .

[45]  Sumio Watanabe,et al.  Asymptotic Equivalence of Bayes Cross Validation and Widely Applicable Information Criterion in Singular Learning Theory , 2010, J. Mach. Learn. Res..

[46]  Benoit B. Mandelbrot,et al.  Fractal Geometry of Nature , 1984 .

[47]  E. Ranta,et al.  Synchronous dynamics and rates of extinction in spatially structured populations , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[48]  S. Peckham,et al.  A reformulation of Horton's Laws for large river networks in terms of statistical self‐similarity , 1999 .

[49]  T. Quinn,et al.  Population dynamics and asynchrony at fine spatial scales: a case history of sockeye salmon (Oncorhynchus nerka) population structure in Alaska, USA , 2012 .

[50]  J. Nichols,et al.  Use of multiple dispersal pathways facilitates amphibian persistence in stream networks , 2010, Proceedings of the National Academy of Sciences.

[51]  Dénes Schmera,et al.  Network thinking in riverscape conservation – A graph-based approach , 2011 .

[52]  Jonathan M. Chase,et al.  The metacommunity concept: a framework for multi-scale community ecology , 2004 .

[53]  D. Post,et al.  The Role of Discharge Variation in Scaling of Drainage Area and Food Chain Length in Rivers , 2010, Science.

[54]  Emanuel A. Fronhofer,et al.  Dendritic network structure and dispersal affect temporal dynamics of diversity and species persistence , 2015 .

[55]  J. Olden,et al.  Homogenization of regional river dynamics by dams and global biodiversity implications , 2007, Proceedings of the National Academy of Sciences.

[56]  V. Gupta,et al.  Random self‐similar river networks and derivations of generalized Horton Laws in terms of statistical simple scaling , 2000 .

[57]  D. Tilman,et al.  Biodiversity and Ecosystem Functioning , 2014 .

[58]  M. D. de Aguiar,et al.  Synchronisation and stability in river metapopulation networks. , 2014, Ecology letters.

[59]  Marc Kery,et al.  Introduction to WinBUGS for Ecologists: Bayesian approach to regression, ANOVA, mixed models and related analyses , 2010 .

[60]  David Steven Scott,et al.  Emergent stability in a large, free-flowing watershed. , 2015, Ecology.

[61]  D. Moss,et al.  Spatial synchrony and asynchrony in butterfly population dynamics , 1996 .

[62]  R. Beverton,et al.  On the dynamics of exploited fish populations , 1993, Reviews in Fish Biology and Fisheries.

[63]  N. Dulvy,et al.  Ecological prophets: quantifying metapopulation portfolio effects , 2013 .

[64]  J. Junker,et al.  River fragmentation increases localized population genetic structure and enhances asymmetry of dispersal in bullhead (Cottus gobio) , 2012, Conservation Genetics.

[65]  W. Fagan CONNECTIVITY, FRAGMENTATION, AND EXTINCTION RISK IN DENDRITIC METAPOPULATIONS , 2002 .

[66]  Ian P. Woiwod,et al.  Spatial synchrony in the dynamics of moth and aphid populations , 1993 .

[67]  Wei Shen,et al.  JMFit: A SAS Macro for Joint Models of Longitudinal and Survival Data. , 2016, Journal of statistical software.

[68]  R. Hilborn,et al.  Population diversity and the portfolio effect in an exploited species , 2010, Nature.

[69]  J. Tonkin,et al.  Metacommunity structuring in Himalayan streams over large elevational gradients: the role of dispersal routes and niche characteristics , 2017 .

[70]  Andrew Gelman,et al.  Data Analysis Using Regression and Multilevel/Hierarchical Models , 2006 .

[71]  A. Maritan,et al.  Evolution and selection of river networks: Statics, dynamics, and complexity , 2014, Proceedings of the National Academy of Sciences.

[72]  Daniel R. Miller,et al.  The Network Dynamics Hypothesis: How Channel Networks Structure Riverine Habitats , 2004 .