Can epidemic control be achieved by altering landscape connectivity in agricultural systems

Few investigations on host diversification at the landscape scale to control plant disease in agricultural systems are available in the literature. At this scale, landscape connectivity measures how the landscape structure facilitates or impedes the disease spread among host patches. We developed a simulation model, giving a particular attention to the representation of the landscape structures, and we characterized the landscape connectivity by the proportion and the aggregation level of the host varieties, the ability for the pathogen to develop on each host and its ability to disperse. The pathogen dynamics was represented by a matrix population model designed for a generic air-borne foliar disease. This framework was used to establish a detailed assessment of the influence of each landscape connectivity variable on the pathogen population dynamics. When deploying a host with complete resistance to the pathogen along with a susceptible host, mixed landscapes were always found to be more efficient to hamper the disease spread. However, when using a quantitatively resistant host, aggregating the hosts in different regions could result in a better control of the pathogen spread, depending on the proportion and level of resistance of the resistant host and according to a source–sink dynamics between the two hosts. The ability of the pathogen to disperse did not change the results from a qualitative point of view. By accounting explicitly for the landscape features, our approach can be used to guide further data analysis or to evaluate the effectiveness of control strategies designed at the landscape scale.

[1]  Laurence V. Madden,et al.  The study of plant disease epidemics , 2007 .

[2]  Manuel Plantegenest,et al.  Landscape epidemiology of plant diseases , 2007, Journal of The Royal Society Interface.

[3]  Ross K. Meentemeyer,et al.  Effects of landscape heterogeneity on the emerging forest disease sudden oak death , 2007 .

[4]  J. Cronin From population sources to sieves: the matrix alters host-parasitoid source-sink structure. , 2007, Ecology.

[5]  D. Hiebeler,et al.  Habitat association in populations on landscapes with continuous-valued heterogeneous habitat quality. , 2013, Journal of theoretical biology.

[6]  Andreas Huth,et al.  Statistical inference for stochastic simulation models--theory and application. , 2011, Ecology letters.

[7]  Xiang-ming Xu A simulation study on managing plant diseases by systematically altering spatial positions of cultivar mixture components between seasons , 2011 .

[8]  Xiangming Xu,et al.  Networks in plant epidemiology: from genes to landscapes, countries, and continents. , 2011, Phytopathology.

[9]  David B. Lindenmayer,et al.  Importance of matrix habitats in maintaining biological diversity , 2009, Proceedings of the National Academy of Sciences.

[10]  A. Hirzel,et al.  Habitat-quality effects on metapopulation dynamics in greater white-toothed shrews, Crocidura russula. , 2008, Ecology.

[11]  J. Metzger,et al.  Importance of estimating matrix quality for modeling species distribution in complex tropical landscapes: a test with Atlantic forest small mammals , 2008 .

[12]  L. Frézal,et al.  Local dispersal of Puccinia triticina and wheat canopy structure. , 2009, Phytopathology.

[13]  S. Soubeyrand,et al.  Autoinfection in wheat leaf rust epidemics. , 2008, The New phytologist.

[14]  Noriko Kinezaki,et al.  The effect of the spatial configuration of habitat fragmentation on invasive spread. , 2010, Theoretical population biology.

[15]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[16]  L. Boitani,et al.  Effect of habitat amount, configuration and quality in fragmented landscapes , 2012 .

[17]  J. Burdon,et al.  Influence of spatial structure on pathogen colonization and extinction: a test using an experimental metapopulation , 2003 .

[18]  C. Mundt,et al.  Landscape heterogeneity and disease spread: experimental approaches with a plant pathogen. , 2011, Ecological applications : a publication of the Ecological Society of America.

[19]  C. Mundt,et al.  Effect of host genotype unit area on development of focal epidemics of bean rust and common maize rust in mixtures of resistant and susceptible plants , 1986 .

[20]  R. Holt,et al.  Meta‐ecosystems: a theoretical framework for a spatial ecosystem ecology , 2003 .

[21]  Hervé Monod,et al.  Pathogen population dynamics in agricultural landscapes: the Ddal modelling framework. , 2014, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[22]  Boris Schröder,et al.  Population dynamics and habitat connectivity affecting the spatial spread of populations – a simulation study , 2004, Landscape Ecology.

[23]  C. Mundt Use of multiline cultivars and cultivar mixtures for disease management. , 2002, Annual review of phytopathology.

[24]  H. Monod,et al.  Dynamics of Adaptation in Spatially Heterogeneous Metapopulations , 2013, PloS one.

[25]  J. N. Perry,et al.  Simulation scenarios of spatio-temporal arrangement of crops at the landscape scale , 2010, Environ. Model. Softw..

[26]  C. Mundt,et al.  Computerized simulation of crown rust epidemics in mixtures of immune and susceptible oat plants with different genotype unit areas and spatial distributions of initial disease , 1986 .

[27]  Mike J Jeger,et al.  Modelling disease spread and control in networks: implications for plant sciences. , 2007, The New phytologist.

[28]  D. Driscoll,et al.  Conceptual domain of the matrix in fragmented landscapes. , 2013, Trends in ecology & evolution.

[29]  Karen A. Garrett,et al.  Connectivity of the American Agricultural Landscape: Assessing the National Risk of Crop Pest and Disease Spread , 2009 .

[30]  H. Monod,et al.  Influence of cultivated landscape composition on variety resistance: an assessment based on wheat leaf rust epidemics. , 2011, The New phytologist.

[31]  Youyong Zhu,et al.  Genetic diversity and disease control in rice , 2000, Nature.

[32]  Saltelli Andrea,et al.  Global Sensitivity Analysis: The Primer , 2008 .

[33]  O. Holdenrieder,et al.  Susceptibility to Fungal Pathogens of Forests Differing in Tree Diversity , 2005 .

[34]  L. Fahrig,et al.  Connectivity is a vital element of landscape structure , 1993 .

[35]  Christopher A Gilligan,et al.  Impact of scale on the effectiveness of disease control strategies for epidemics with cryptic infection in a dynamical landscape: an example for a crop disease , 2007, Journal of The Royal Society Interface.

[36]  Sabrina Gaba,et al.  Combined use of local and ANOVA-based global sensitivity analyses for the investigation of a stochastic dynamic model: Application to the case study of an individual-based model of a fish population , 2006 .

[37]  L. Fahrig Effects of Habitat Fragmentation on Biodiversity , 2003 .

[38]  T. Johnson Man-Guided Evolution in Plant Rusts: Through his modification of the host plants of the cereal rusts, man is also modifying the rusts. , 1961, Science.

[39]  J. Elkinton,et al.  Spatial Scale and the Spread of a Fungal Pathogen of Gypsy Moth , 1998, The American Naturalist.

[40]  A. Bennett,et al.  Meeting the demand for crop production: the challenge of yield decline in crops grown in short rotations , 2012, Biological reviews of the Cambridge Philosophical Society.

[41]  P. Holgate,et al.  Matrix Population Models. , 1990 .

[42]  C. Mundt,et al.  Effect of host genotype unit area on epidemic development of crown rust following focal and general inoculations of mixtures of immune and susceptible oat plants , 1985 .

[43]  Atsuyuki Okabe,et al.  Spatial Tessellations: Concepts and Applications of Voronoi Diagrams , 1992, Wiley Series in Probability and Mathematical Statistics.

[44]  D. Isaak,et al.  Chinook salmon use of spawning patches: relative roles of habitat quality, size, and connectivity. , 2007, Ecological applications : a publication of the Ecological Society of America.

[45]  Alison G. Power,et al.  Pathogen Spillover in Disease Epidemics , 2004, The American Naturalist.

[46]  C. Gilligan,et al.  Large-scale fungicide spray heterogeneity and the regional spread of resistant pathogen strains. , 2006, Phytopathology.

[47]  K. Garrett,et al.  Epidemiology in mixed host populations. , 1999, Phytopathology.

[48]  S. Gandon,et al.  Evolution of specialization in a spatially continuous environment , 2010, Journal of evolutionary biology.

[49]  K. Frey,et al.  Multiline Cultivars as a Means of Disease Control , 1969 .

[50]  R. Schooley,et al.  Spatial Heterogeneity in Habitat Quality and Cross-Scale Interactions in Metapopulations , 2007, Ecosystems.

[51]  Shuangzhe Liu,et al.  Global Sensitivity Analysis: The Primer by Andrea Saltelli, Marco Ratto, Terry Andres, Francesca Campolongo, Jessica Cariboni, Debora Gatelli, Michaela Saisana, Stefano Tarantola , 2008 .

[52]  M. Beaumont Approximate Bayesian Computation in Evolution and Ecology , 2010 .

[53]  R. Ostfeld,et al.  Effects of species diversity on disease risk. , 2006, Ecology letters.

[54]  Andrew S. Pullin,et al.  A meta-analysis on the impact of different matrix structures on species movement rates , 2012, Landscape Ecology.

[55]  W. Rossing,et al.  Influence of host diversity on development of epidemics: an evaluation and elaboration of mixture theory. , 2005, Phytopathology.

[56]  H. Monod,et al.  Assessing Four-Way Mixtures of Winter Wheat Cultivars from the Performances of their Two-Way and Individual Components , 2006, European Journal of Plant Pathology.

[57]  Luigi Boitani,et al.  The role of habitat quality in fragmented landscapes: a conceptual overview and prospectus for future research , 2010, Oecologia.

[58]  F. van den Bosch,et al.  Spread of organisms: can travelling and dispersive waves be distinguished? , 2000 .

[59]  L. Madden,et al.  Rothamsted Repository Download , 2022 .

[60]  Marcus Vinícius Vieira,et al.  Does the type of matrix matter? A quantitative review of the evidence , 2010, Biodiversity and Conservation.

[61]  R. Schooley,et al.  Enhancing the area-isolation paradigm: habitat heterogeneity and metapopulation dynamics of a rare wetland mammal. , 2009, Ecological applications : a publication of the Ecological Society of America.

[62]  C. Mundt,et al.  Analysis of Factors Affecting Disease Increase and Spread in Mixtures of Immune and Susceptible Plants in Computer-Simulated Epidemics , 1986 .

[63]  Karen A. Garrett,et al.  Why dispersal should be maximized at intermediate scales of heterogeneity , 2012, Theoretical Ecology.

[64]  James F. Meadow,et al.  Importance of dispersal and thermal environment for mycorrhizal communities: lessons from Yellowstone National Park. , 2011, Ecology.

[65]  C. Mundt,et al.  The effects of dispersal gradient and pathogen life cycle components on epidemic velocity in computer simulations. , 2005, Phytopathology.

[66]  P. Gouyon,et al.  Mixing of propagules from discrete sources at long distance: comparing a dispersal tail to an exponential , 2006, BMC Ecology.

[67]  P. Whigham,et al.  Functional connectivity and matrix quality: network analysis for a critically endangered New Zealand lizard , 2013, Landscape Ecology.

[68]  C. Mundt,et al.  Primary disease gradients of wheat stripe rust in large field plots. , 2005, Phytopathology.

[69]  A. Zeileis,et al.  Beta Regression in R , 2010 .

[70]  J. R. Hardison Fire and Flame for Plant Disease Control , 1976 .

[71]  Wopke van der Werf,et al.  Invasion of Phytophthora infestans at the landscape level: how do spatial scale and weather modulate the consequences of spatial heterogeneity in host resistance? , 2010, Phytopathology.

[72]  Mark W. Schwartz,et al.  Choosing the Appropriate Scale of Reserves for Conservation , 1999 .

[73]  G. McDonald,et al.  Effects of crop rotation, residue retention and sowing time on the incidence and survival of ascochyta blight and its effect on grain yield of field peas (Pisum sativum L.). , 2009 .

[74]  K. Kiêu,et al.  A completely random T-tessellation model and Gibbsian extensions , 2013, 1302.1809.

[75]  Christian Lannou,et al.  Variation and selection of quantitative traits in plant pathogens. , 2012, Annual review of phytopathology.

[76]  T. Fartmann,et al.  Effects of landscape and habitat quality on butterfly communities in pre-alpine calcareous grasslands , 2012 .

[77]  Bruno Sudret,et al.  Global sensitivity analysis using polynomial chaos expansions , 2008, Reliab. Eng. Syst. Saf..

[78]  K. Garrett,et al.  Pest and Disease Management: Why We Shouldn't Go against the Grain , 2013, PloS one.

[79]  E. Stukenbrock,et al.  The origins of plant pathogens in agro-ecosystems. , 2008, Annual review of phytopathology.

[80]  Hervé Monod,et al.  Computation of the integrated flow of particles between polygons , 2009, Environ. Model. Softw..

[81]  C. Gilligan,et al.  Measures of durability of resistance. , 2003, Phytopathology.

[82]  R. Ricklefs,et al.  Community Diversity: Relative Roles of Local and Regional Processes , 1987, Science.