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Epidemiological modeling of
  Phytophthora ramorum: network
properties of susceptible plant genera
movements in the UK nursery sector
 Marco Pautasso,1 Tom Harwood,2 Mike Shaw,2
        Xiangming Xu3 & Mike Jeger1

       1 Imperial College London, UK
         2 University of Reading, UK
         3 East Malling Research, UK

            SOD Symposium III,
               8 Mar 2007
Disease spread in
                                                                 a globalized world




                            number of passengers per day
From: Hufnagel, Brockmann & Geisel (2004) Forecast and control
of epidemics in a globalized world. PNAS 101: 15124-15129
Epidemiology is just one of the
              many applications of network theory
Network pictures from:
Newman (2003)                   NATURAL
The structure and function
of complex networks.                        food webs
SIAM Review 45: 167-256
                                          cell
                                       metabolism
                                               neural                           Food web of Little Rock
                                              networks                            Lake, Wisconsin, US
                                             ant nests           sexual
                                                              partnerships
                                            DISEASE
                                            SPREAD
                                                               family
                                     innovation               networks
Internet                                flows co-authorship                                      HIV
structure                     railway urban road nets                                          spread
                 electrical  networks networks                                                network
               power grids                                telephone calls
                                                WWW
          computing          airport Internet              E-mail
                                                                     committees
            grids           networks     software maps    patterns
TECHNOLOGICAL                                                                         SOCIAL
Modified from: Jeger MJ, Pautasso M, Holdenrieder O & Shaw MW (2007) Modelling disease
spread and control in networks: implications for plant sciences. New Phytologist in press
Different types of networks




      local                                small-world




                        random                              scale-free

Modified from: Keeling & Eames (2005) Networks and epidemic models. Interface 2: 295-307
Epidemic development in different types of networks



                                                                    scale-free
                                                                    random
                                                                    2-D lattice rewired
                                                                    2-D lattice
                                                                    1-D lattice rewired
                                                                    1-D lattice

                                                          N of nodes of networks = 500;
                                                                p of infection = 0.1;
                                                           latent period = 2 time steps;
                                                         infectious period = 10 time steps




   From: Shirley & Rushton (2005) The impacts of network topology on disease spread.
                            Ecological Complexity 2: 287-299
Temporal development; England & Wales, 2003-2005; n = 1104
                 100
                                     Records positive to P. ramorum

                  75                                                           nurseries/
  n of records



                                                                               garden
                                                                               centres
                  50


                  25


                      0
                                    3




                                                            4




                                                                                    5
                  03




                                        3
                                             04




                                                                4
                                                                     05




                                                                                        5
                           3




                                                   4




                                                                            5
                          -0




                                                   -0




                                                                            -0
                               l-0




                                                        l-0




                                                                                 l-0
                                        -0




                                                                -0




                                                                                        -0
                 n-




                                             n-




                                                                     n-
                          pr




                                                  pr




                                                                          pr
                                     ct




                                                              ct




                                                                                       ct
                               Ju




                                                       Ju




                                                                               Ju
                 Ja




                                          Ja




                                                                   Ja
                                    O




                                                            O




                                                                                    O
                      A




                                               A




                                                                        A
Data source: Department for Environment, Food and Rural Affairs, UK
Temporal development; England & Wales, 2003-2005; n = 1456
                250
                                     Records positive to P. ramorum
                200
                                   estates/
 n of records



                                   environment
                150

                100

                 50

                     0
                                   3




                                                           4




                                                                                   5
                 03




                                            04




                                                                     05
                                                                4




                                                                                         5
                                       3
                          3




                                                   4




                                                                             5
                         -0




                                                   -0




                                                                             -0
                              l -0




                                                        l -0




                                                                                  l-0
                                                               -0




                                                                                        -0
                                       -0
                n-




                                            n-




                                                                    n-
                         pr




                                                 pr




                                                                         pr
                                                               ct




                                                                                        ct
                                     ct
                              Ju




                                                      Ju




                                                                              Ju
                Ja




                                          Ja




                                                                    Ja
                                   O




                                                           O




                                                                                   O
                     A




                                               A




                                                                         A
Data source: Department for Environment, Food and Rural Affairs, UK
Temporal development; England & Wales, 2003-2005; n = 704
                           Nursery records positive to P. ramorum
               100%

                                      UK origin
               75%                    non-UK origin
n of records




               50%


               25%


                0%
                        3




                                                  4




                                                                          5
                                3




                                                         4




                                                                                   5
                                     3




                                                               4




                                                                                       5
                 03




                                          04




                                                                    05
                        -0




                                                  -0




                                                                         -0
                             l-0




                                                       l-0




                                                                              l-0
                                     -0




                                                               -0




                                                                                      -0
                n-




                                          n-




                                                                    n-

                                                                         pr
                      pr




                                               pr
                                   ct




                                                             ct




                                                                                    ct
                           Ju




                                                    Ju




                                                                              Ju
               Ja




                                      Ja




                                                                Ja
                                O




                                                         O




                                                                                   O
                    A




                                           A




                                                                     A
Data source: Department for Environment, Food and Rural Affairs, UK
England and Wales: records positive
                      to Phytophthora ramorum
                              n = 2788
                               Jan 2003-Dec 2005




Courtesy of
Richard Baker,                 Data source: DEFRA, UK
CSL, UK
Web of susceptible genera connected by Phytophthora ramorum (based on
genus co-existence in 2788 positive findings in England & Wales, 2003-2005)
                               Viburnum
                  Camellia                     Umbellularia

          Castanea                                        Taxus

                                                             Syringa
      Drimys

     Fagus                                                    Rhodo-
                                                              dendron
     Festuca

  Hamamelis                                                   Quercus

        Kalmia                                             Pieris
               Laurus                     Magnolia Parrotia
                           Leucothoe

Data source: DEFRA, UK
Frequency distribution of number of plant genera affected by
 Phytophthora ramorum by n of records in the database of 2788
      positive findings in England & Wales, 2003-2005)
                                      1.2
    log10 number of affected genera


                                                                                 y = -0.33x + 1.27
                                      1.0                                              2
                                                                                     R = 0.93
                                      0.8

                                      0.6

                                      0.4

                                      0.2

                                      0.0
                                            0.0             1.0           2.0            3.0           4.0
                                                  log10 n of positive P. ramorum records in database
Data source: DEFRA, UK
Connectivity loss in the North American power grid
    due to the removal of transmission substations




                                transmission nodes removed (%)

From: Albert, Albert & Nakarado (2004) Structural vulnerability of the
      North American power grid. Physical Review E 69, 025103
Acknowledgements
Alan Inman, Department for Environment, Food
            and Rural Affairs, UK

       Claire Sansford, Judith Turner
              & Richard Baker,
    Central Science Laboratory, York, UK

       Sandra Denman & Joan Webber,
       Forest Research, Alice Holt, UK

    Ottmar Holdenrieder, ETH, Zurich, CH

   Jennifer Parke, Oregon State University
References
Dehnen-Schmutz K, Holdenrieder O, Jeger MJ & Pautasso M (2010) Structural change in the international horticultural industry: some implications
for plant health. Scientia Horticulturae 125: 1-15
Harwood TD, Xu XM, Pautasso M, Jeger MJ & Shaw M (2009) Epidemiological risk assessment using linked network and grid based modelling:
Phytophthora ramorum and P. kernoviae in the UK. Ecological Modelling 220: 3353-3361
Jeger MJ & Pautasso M (2008) Comparative epidemiology of zoosporic plant pathogens. European Journal of Plant Pathology 122: 111-126
Jeger MJ, Pautasso M, Holdenrieder O & Shaw MW (2007) Modelling disease spread and control in networks: implications for plant sciences. New
Phytologist 174: 179-197
Lonsdale D, Pautasso M & Holdenrieder O (2008) Wood-decaying fungi in the forest: conservation needs and management options. European
Journal of Forest Research 127: 1-22
MacLeod A, Pautasso M, Jeger MJ & Haines-Young R (2010) Evolution of the international regulation of plant pests and challenges for future plant
health. Food Security 2: 49-70
Moslonka-Lefebvre M, Pautasso M & Jeger MJ (2009) Disease spread in small-size directed networks: epidemic threshold, correlation between
links to and from nodes, and clustering. J Theor Biol 260: 402-411
Moslonka-Lefebvre M, Finley A, Dorigatti I, Dehnen-Schmutz K, Harwood T, Jeger MJ, Xu XM, Holdenrieder O & Pautasso M (2011) Networks in
plant epidemiology: from genes to landscapes, countries and continents. Phytopathology 101: 392-403
Pautasso M (2009) Geographical genetics and the conservation of forest trees. Perspectives in Plant Ecology, Systematics & Evolution 11: 157-189
Pautasso M (2010) Worsening file-drawer problem in the abstracts of natural, medical and social science databases. Scientometrics 85: 193-202
Pautasso M & Jeger MJ (2008) Epidemic threshold and network structure: the interplay of probability of transmission and of persistence in directed
networks. Ecological Complexity 5: 1-8
Pautasso M et al (2010) Plant health and global change – some implications for landscape management. Biological Reviews 85: 729-755
Pautasso M, Moslonka-Lefebvre M & Jeger MJ (2010) The number of links to and from the starting node as a predictor of epidemic size in small-
size directed networks. Ecological Complexity 7: 424-432
Pautasso M, Xu XM, Jeger MJ, Harwood T, Moslonka-Lefebvre M & Pellis L (2010) Disease spread in small-size directed trade networks: the role of
hierarchical categories. Journal of Applied Ecology 47: 1300-1309
Xu XM, Harwood TD, Pautasso M & Jeger MJ (2009) Spatio-temporal analysis of an invasive plant pathogen (Phytophthora ramorum) in England
and Wales. Ecography 32: 504-516

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Epidemiological modeling of Phytophthora ramorum spread in UK nurseries

  • 1. Epidemiological modeling of Phytophthora ramorum: network properties of susceptible plant genera movements in the UK nursery sector Marco Pautasso,1 Tom Harwood,2 Mike Shaw,2 Xiangming Xu3 & Mike Jeger1 1 Imperial College London, UK 2 University of Reading, UK 3 East Malling Research, UK SOD Symposium III, 8 Mar 2007
  • 2. Disease spread in a globalized world number of passengers per day From: Hufnagel, Brockmann & Geisel (2004) Forecast and control of epidemics in a globalized world. PNAS 101: 15124-15129
  • 3. Epidemiology is just one of the many applications of network theory Network pictures from: Newman (2003) NATURAL The structure and function of complex networks. food webs SIAM Review 45: 167-256 cell metabolism neural Food web of Little Rock networks Lake, Wisconsin, US ant nests sexual partnerships DISEASE SPREAD family innovation networks Internet flows co-authorship HIV structure railway urban road nets spread electrical networks networks network power grids telephone calls WWW computing airport Internet E-mail committees grids networks software maps patterns TECHNOLOGICAL SOCIAL Modified from: Jeger MJ, Pautasso M, Holdenrieder O & Shaw MW (2007) Modelling disease spread and control in networks: implications for plant sciences. New Phytologist in press
  • 4. Different types of networks local small-world random scale-free Modified from: Keeling & Eames (2005) Networks and epidemic models. Interface 2: 295-307
  • 5. Epidemic development in different types of networks scale-free random 2-D lattice rewired 2-D lattice 1-D lattice rewired 1-D lattice N of nodes of networks = 500; p of infection = 0.1; latent period = 2 time steps; infectious period = 10 time steps From: Shirley & Rushton (2005) The impacts of network topology on disease spread. Ecological Complexity 2: 287-299
  • 6. Temporal development; England & Wales, 2003-2005; n = 1104 100 Records positive to P. ramorum 75 nurseries/ n of records garden centres 50 25 0 3 4 5 03 3 04 4 05 5 3 4 5 -0 -0 -0 l-0 l-0 l-0 -0 -0 -0 n- n- n- pr pr pr ct ct ct Ju Ju Ju Ja Ja Ja O O O A A A Data source: Department for Environment, Food and Rural Affairs, UK
  • 7. Temporal development; England & Wales, 2003-2005; n = 1456 250 Records positive to P. ramorum 200 estates/ n of records environment 150 100 50 0 3 4 5 03 04 05 4 5 3 3 4 5 -0 -0 -0 l -0 l -0 l-0 -0 -0 -0 n- n- n- pr pr pr ct ct ct Ju Ju Ju Ja Ja Ja O O O A A A Data source: Department for Environment, Food and Rural Affairs, UK
  • 8. Temporal development; England & Wales, 2003-2005; n = 704 Nursery records positive to P. ramorum 100% UK origin 75% non-UK origin n of records 50% 25% 0% 3 4 5 3 4 5 3 4 5 03 04 05 -0 -0 -0 l-0 l-0 l-0 -0 -0 -0 n- n- n- pr pr pr ct ct ct Ju Ju Ju Ja Ja Ja O O O A A A Data source: Department for Environment, Food and Rural Affairs, UK
  • 9. England and Wales: records positive to Phytophthora ramorum n = 2788 Jan 2003-Dec 2005 Courtesy of Richard Baker, Data source: DEFRA, UK CSL, UK
  • 10. Web of susceptible genera connected by Phytophthora ramorum (based on genus co-existence in 2788 positive findings in England & Wales, 2003-2005) Viburnum Camellia Umbellularia Castanea Taxus Syringa Drimys Fagus Rhodo- dendron Festuca Hamamelis Quercus Kalmia Pieris Laurus Magnolia Parrotia Leucothoe Data source: DEFRA, UK
  • 11. Frequency distribution of number of plant genera affected by Phytophthora ramorum by n of records in the database of 2788 positive findings in England & Wales, 2003-2005) 1.2 log10 number of affected genera y = -0.33x + 1.27 1.0 2 R = 0.93 0.8 0.6 0.4 0.2 0.0 0.0 1.0 2.0 3.0 4.0 log10 n of positive P. ramorum records in database Data source: DEFRA, UK
  • 12. Connectivity loss in the North American power grid due to the removal of transmission substations transmission nodes removed (%) From: Albert, Albert & Nakarado (2004) Structural vulnerability of the North American power grid. Physical Review E 69, 025103
  • 13. Acknowledgements Alan Inman, Department for Environment, Food and Rural Affairs, UK Claire Sansford, Judith Turner & Richard Baker, Central Science Laboratory, York, UK Sandra Denman & Joan Webber, Forest Research, Alice Holt, UK Ottmar Holdenrieder, ETH, Zurich, CH Jennifer Parke, Oregon State University
  • 14. References Dehnen-Schmutz K, Holdenrieder O, Jeger MJ & Pautasso M (2010) Structural change in the international horticultural industry: some implications for plant health. Scientia Horticulturae 125: 1-15 Harwood TD, Xu XM, Pautasso M, Jeger MJ & Shaw M (2009) Epidemiological risk assessment using linked network and grid based modelling: Phytophthora ramorum and P. kernoviae in the UK. Ecological Modelling 220: 3353-3361 Jeger MJ & Pautasso M (2008) Comparative epidemiology of zoosporic plant pathogens. European Journal of Plant Pathology 122: 111-126 Jeger MJ, Pautasso M, Holdenrieder O & Shaw MW (2007) Modelling disease spread and control in networks: implications for plant sciences. New Phytologist 174: 179-197 Lonsdale D, Pautasso M & Holdenrieder O (2008) Wood-decaying fungi in the forest: conservation needs and management options. European Journal of Forest Research 127: 1-22 MacLeod A, Pautasso M, Jeger MJ & Haines-Young R (2010) Evolution of the international regulation of plant pests and challenges for future plant health. Food Security 2: 49-70 Moslonka-Lefebvre M, Pautasso M & Jeger MJ (2009) Disease spread in small-size directed networks: epidemic threshold, correlation between links to and from nodes, and clustering. J Theor Biol 260: 402-411 Moslonka-Lefebvre M, Finley A, Dorigatti I, Dehnen-Schmutz K, Harwood T, Jeger MJ, Xu XM, Holdenrieder O & Pautasso M (2011) Networks in plant epidemiology: from genes to landscapes, countries and continents. Phytopathology 101: 392-403 Pautasso M (2009) Geographical genetics and the conservation of forest trees. Perspectives in Plant Ecology, Systematics & Evolution 11: 157-189 Pautasso M (2010) Worsening file-drawer problem in the abstracts of natural, medical and social science databases. Scientometrics 85: 193-202 Pautasso M & Jeger MJ (2008) Epidemic threshold and network structure: the interplay of probability of transmission and of persistence in directed networks. Ecological Complexity 5: 1-8 Pautasso M et al (2010) Plant health and global change – some implications for landscape management. Biological Reviews 85: 729-755 Pautasso M, Moslonka-Lefebvre M & Jeger MJ (2010) The number of links to and from the starting node as a predictor of epidemic size in small- size directed networks. Ecological Complexity 7: 424-432 Pautasso M, Xu XM, Jeger MJ, Harwood T, Moslonka-Lefebvre M & Pellis L (2010) Disease spread in small-size directed trade networks: the role of hierarchical categories. Journal of Applied Ecology 47: 1300-1309 Xu XM, Harwood TD, Pautasso M & Jeger MJ (2009) Spatio-temporal analysis of an invasive plant pathogen (Phytophthora ramorum) in England and Wales. Ecography 32: 504-516