Consequences of long-distance dispersal for epidemic spread: Patterns, scaling, and mitigation

Plant Disease

Volumn 103, Issue 2, 2019, Pages 177-191

  Severns, Paul M ^a   Sackett, Kathryn E ^a   Farber, Daniel H ^a,b   Mundt, Christopher C ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BASIDIOMYCETES; BIOLOGICAL MODEL; COMPUTER SIMULATION; HUMAN; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PREVENTION AND CONTROL;

ANIMALS; BASIDIOMYCOTA; COMPUTER SIMULATION; HUMANS; MODELS, BIOLOGICAL; PLANT DISEASES;

EID: 85060554501     PISSN: 01912917     EISSN: 19437692     Source Type: Journal    
DOI: 10.1094/PDIS-03-18-0505-FE     Document Type: Article

References (130)

1. Altizer, S., Ostfleld, R. S., Johnson, P. T. J., Kutz, S., and Harvell, C. D. 2013. Climate change and infectious diseases: from evidence to a predictive framework. Science 341:514-519.
2. Anderson, P. K., Cunningham, A. A., Patel, N. G., Morales, F. J., Epstein, P. R., and Daszak, P. 2004. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol. Evol. 19: 535-544.
3. Ausubel, F. M. 2005. Are innate immune signaling pathways in plants and animals conserved? Nat. Immunol. 6:973-979.
4. Aylor, D. E. 2017. Aerial Dispersal of Pollen and Spores. APS Press, St. Paul, MN.
5. Aylor, D. E., and Ferrandino, F. J. 1989. Temporal and spatial development of bean rust epidemics initiated from an inoculated line source. Phytopathology 79:146-151.
6. Bjornstad, O. N., Peltonen, M., Liebhold, A. M., and Batlensweiler, W. 2002. Waves of larch budmoth outbreaks in the European Alps. Science 298: 1020-1023.
7. Borer, E. T., Antonovics, J., Kinkel, L. L., Hudson, P. J., Daszak, P., Ferrari, M. J., Garrett, K. A., Parrish, C. R., Read, A. F., and Rizzo, D. M. 2011. Bridging taxonomic and disciplinary divides in infectious disease. EcoHealth 8:261-267.
8. Boudreau, M. A., and Mundt, C. C. 1994. Mechanisms of alteration in bean rust development due to intercropping, in computer-simulated epidemics. Ecol. Appl. 4:729-740.
9. Bourke, P. M. A. 1964. Emergence of potato blight, 1843–1846. Nature 203: 805-808.
10. Brockmann, D., Hufnagel, L., and Geisel, T. 2006. The scaling laws of human travel. Nature 439:462-465.
11. Brown, D. H., and Bolker, B. M. 2004. The effects of disease dispersal and host clustering on the epidemic threshold in plants. Bull. Math. Biol. 66:341-371.
12. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M., and West, G. B. 2004. Toward a metabolic theory of ecology. Ecology 85:1771-1789.
13. Brown, J. K. M., and Hovmøller, M. S. 2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297: 537-541.
14. Chave, J. 2013. The problem of pattern and scale in ecology: what have we learned in 20 years? Ecol. Lett. 16:4-16.
15. Chen, W., Wellings, C., Chen, X., Kang, Z., and Liu, T. 2014. Wheat stripe (yellow) rust caused by Puccinia striiformis f. sp. tritici. Mol. Plant Pathol. 15:433-446.
16. Chen, X. M., Moore, M., Milus, E. A., Long, D. L., Line, R. F., Marshall, D., and Jackson, L. 2002. Wheat stripe rust epidemics and races of Puccinia striiformis f. sp. tritici in the United States in 2000. Plant Dis. 86:39-46.
17. Chis Ster, I., and Ferguson, N. M. 2007. Transmission parameters of the 2001 foot and mouth epidemic in Great Britain. PLoS One 2:e502.
18. Clark, J. S., Lewis, M., and Horvath, L. 2001. Invasion by extremes: Population spread with variation in dispersal and reproduction. Am. Nat. 157:537-554.
19. Clobert, J., Baguette, M., Benton, T. G., and Bullock, J. M., eds. 2012. Dispersal ecology and evolution. Oxford University Press, Oxford, UK.
20. Cowger, C., Wallace, L. D., and Mundt, C. C. 2005. Velocity of spread of wheat stripe rust epidemics. Phytopathology 95:972-982.
21. Crowl, T. A., Crist, T. O., Parmenter, R. R., Belovsky, G., and Lugo, A. E. 2008. The spread of invasive species and infectious disease as drivers of ecosystem change. Front. Ecol. Environ. 6:238-246.
22. Cummings, D. A. T., Irizarry, R. A., Huang, N. E., Endy, T. P., Nisalak, A., Ungchusak, K., and Burke, D. S. 2004. Travelling waves in the occurrence of dengue haemorrhaic fever in Thailand. Nature 427:344-347.
23. Cunniffe, N. J., Laranjeira, F. F., Neri, F. M., DeSimone, R. E., and Gilligan, C. A. 2014. Cost-effective control of plant disease when epidemiological knowledge is incomplete: modelling Bahia bark scaling of citrus. PLOS Comput. Biol. 10: e1003753.
24. Dybiec, B., Kleczkowski, A., and Gilligan, C. A. 2009. Modelling control of epidemics spreading by long-range interactions. J. R. Soc. Interface 6:941-950.
25. Enquist, B. J., Brown, J. H., and West, G. B. 1998. Allometric scaling of plant energetics and population density. Nature 395:163-165.
26. Estep, L. K., Sackett, K. E., and Mundt, C. C. 2014. Influential disease foci in epidemics and underlying mechanisms: a field experiment and simulations. Ecol. Appl. 24:1854-1862.
27. Eubank, S., Guclu, H., Anil Kumar, V. S., Marathe, M. V., Srinivasan, A., Toroczkai, Z., and Wang, N. 2004. Modelling disease outbreaks in realistic urban social networks. Nature 429:180-184.
28. Farber, D. 2016. The Primary Disease Gradient of Wheat Stripe Rust (Puccinia striiformis f.sp. tritici) Across Spatial Scales. Ph.D. Thesis, Oregon State University, Corvallis, OR.
29. Farber, D. H., Medlock, J., and Mundt, C. C. 2017. Local dispersal of Puccinia striiformis f. sp. tritici from isolated source lesions. Plant Pathol. 66:28-37.
30. Ferrandino, F. J. 1993. Dispersive epidemic waves: I. Focus expansion within a linear planting. Phytopathology 83:795-802.
31. Ferrandino, F. J. 1996. Length scale of disease spread: Fact or artifact of experimental geometry? Phytopathology 86:806-811.
32. Filipe, J. A. N., Cobb, R. C., Meentemeyer, R. K., Lee, C. A., Valachovic, Y. S., Cook, A. R., Rizzo, D. M., and Gilligan, C. A. 2012. Landscape epidemiology and control of pathogens with cryptic and long-distance dispersal: Sudden oak death in northern Californian forests. PLOS Comput. Biol. 8:e1002328.
33. Fisher, M. C., Henk, D. A., Briggs, C. J., Brownstein, J. S., Madoff, L. C., McCraw, S. L., and Gurr, S. G. 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186-194.
34. Fleming, R., Marsh, L., and Tuckwell, H. 1982. Effect of field geometry on the spread of crop disease. Prot. Ecol. 4:81-108.
35. Frantzen, J., and van den Bosch, F. 2000. Spread of organisms: can travelling and dispersive waves be distinguished? Basic Appl. Ecol. 1:83-92.
36. Frezal, L., Robert, C., Bancal, M.-O., and Lannou, C. 2009. Local dispersal of leaf rust and wheat canopy structure. Phytopathology 99:1216-1224.
37. Gisiger, T. 2001. Scale invariance in biology: coincidence or footprint of a universal mechanism? Biol. Rev. 76:161-209.
38. Gregory, P. H. 1968. Interpreting plant disease dispersal gradients. Annu. Rev. Phytopathol. 6:189-212.
39. Grenfell, B. T., Bjornstad, O. N., and Kappey, J. 2001. Travelling waves and spatial hierarchies in measles epidemics. Nature 414:716-723.
40. Harper, J. L. 1977. The Population Biology of Plants. Academic Press, London.
41. Haskell, J. P., Ritchie, M. E., and Olff, H. 2002. Fractal geometry predicts varying body size scaling relationships for mammal and bird home ranges. Nature 418: 527-530.
42. Hastings, A., Cuddington, K., Davies, K. F., Dugaw, C. J., Elmendorf, S., Freestone, A., Harrison, S., Holland, M., Lambrinos, J., Malvadkar, U., Melbourne, B. A., Moore, K., Taylor, C., and Thomson, D. 2005. The spatial spread of invasions: new developments in theory and evidence. Ecol. Lett. 8:91-101.
43. Heesterbeek, J. A. P., and Zadoks, J. C. 1987. Modeling pandemics of quarantine pests and diseases: problems and perspectives. Crop Prot. 6:211-221.
44. Helfer, S. 2014. Rust fungi and global change. New Phytol. 201:770-780.
45. HEWSweb. 2006. Humanitarian Early Warning Service.
46. Jeger, M. J., Pautasso, M., Holdenrieder, O., and Shaw, M. W. 2007. Modelling disease spread and control in networks: implications for plant sciences. New Phytol. 174:279-297.
47. Johnson, D. M., Liebold, A. M., Tobin, P. C., and Bjornstad, O. N. 2006. Allee effects and pulsed invasion by the gypsy moth. Nature 444:361-363.
48. Kampmeijer, P., and Zadoks, J. C. 1977. EPIMUL, a Simulator of Foci and Epidemics in Mixtures of Resistant and Susceptible Plants, Mosaics and Multilines. Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands.
49. Keeling, M. J., Woolhouse, M. E. J., Shaw, D. J., Matthews, L., Chase-Topping, M., Haydon, D. T., Cornell, S. J., Kappey, J., Wilesmith, J., and Grenfell, B. J. 2001. Dynamics of the 2001 UK foot and mouth epidemic: stochastic dispersal in a heterogeneous landscape. Science 294:813-817.
50. Kingsolver, C. H., Peet, C. E., and Underwood, J. F. 1984. Measurement of the Epidemic Potential of Wheat Stem Rust: St. Croix, U.S. Virgin Islands, 1954-1957. Bulletin 854, The Pennsylvania State University, College of Agriculture, Agricultural Experiment Station, University Park, Pennsylvania.
51. Kot, M., Lewis, M. A., and van den Driessche, P. 1996. Dispersal data and the spread of invading organisms. Ecology 77:2027-2042.
52. Kristensen, N. P., Barro, P. J. D., and Schellhorn, N. A. 2013. The initial dispersal and spread of an intentional invader at three spatial scales. PLoS One 8:e62407.
53. Lambin, X., Elston, D. A., Petty, S. J., and MacKinnon, J. L. 1998. Spatial asynchrony and periodic travelling waves in cyclic populations of field voles. Proc. R. Soc. Lond., B 265:1491-1496.
54. Lannou, C., and Mundt, C. C. 1996. Evolution of a pathogen population in host mixtures: simple race-complex race competition. Plant Pathol. 45:440-453.
55. Lannou, C., and Mundt, C. C. 1997. Evolution of a pathogen population in host mixtures: Rate of emergence of complex races. Theor. Appl. Genet. 94:991-999.
56. Lannou, C., Soubeyrand, S., Frezal, L., and Chadoeuf, J. 2008. Autoinfection in wheat leaf rust epidemics. New Phytol. 177:1001-1011.
57. Leclerc, M., Doré, T., Gilligan, C. A., Lucas, P., and Filipe, J. A. N. 2013. Host growth can cause invasive spread of crops by soilborne pathogens. PLoS One 8: e63003.
58. Leonard, K. J., and Szabo, L. J. 2005. Stem rust of small grains and grasses caused by Puccinia graminis. Mol. Plant Pathol. 6:99-111.
59. Levin, S. A. 1992. The problem of pattern and scale in ecology. Ecology 73: 1943-1967.
60. Lindstrӧm, T., Håkansson, N., and Wennergren, U. 2011. The shape of the spatial kernel and its implications for biological invasions in patchy environments. Proc. R. Soc. B 278:1564-1571.
61. Mack, R. N., Simberloff, D., Lonsdale, W. M., Evans, H., Clout, M., and Bazzaz, F. A. 2000. Biotic invasions: causes, epidemiology, global consequences, and control. Ecol. Appl. 10:689-710.
62. Madden, L. V., Hughes, G., and van den Bosch, F. 2007. The Study of Plant Disease Epidemics. APS Press, St. Paul, MN.
63. Margosian, M. L., Garrett, K. A., Hutchinson, J. M. S., and With, K. A. 2009. Connectivity of the American agricultural landscape: Assessing the national risk of crop pest and disease spread. Bioscience 59:141-151.
64. Marquet, P. A., Quiñones, R. A., Abades, S., Labra, F., Tognelli, M., Arim, M., and Rivadeneira, M. 2005. Scaling and power-laws in ecological systems. J. Exp. Biol. 208:1749-1769.
65. McIntire, E. J. B., Rompré, G., and Severns, P. M. 2013. Biased correlated random walk and foray loop: which movement hypothesis drives a butterfly metapopulation. Oecologia 172:293-305.
66. Milne, B. T. 1998. Motivation and beliefs of complex systems approaches in ecology. Ecosystems (N. Y.) 1:449-456.
67. Milus, E. A., Kristensen, K., and Hovmøller, M. S. 2009. Evidence for increased aggressiveness in a recent widespread strain of Puccinia striiformis f. sp. tritici causing stripe rust of wheat. Phytopathology 99:89-94.
68. Minogue, K. P., and Fry, W. E. 1983a. Models for the spread of disease: Model description. Phytopathology 73:1168-1173.
69. Minogue, K. P., and Fry, W. E. 1983b. Models for the spread of plant disease: Some experimental results. Phytopathology 73:1173-1176.
70. Mollison, D. 1977. Spatial contact models for ecological and epidemic spread. J. R. Stat. Soc. B 39:283-326.
71. Moore, W. F. 1970. Origin and spread of southern corn leaf blight in 1970. Plant Dis. Rep. 54:1104-1108.
72. Mundt, C. C. 1989. Use of the modified Gregory model to describe primary disease gradients of wheat leaf rust produced from area sources of inoculum. Phytopathology 79:241-246.
73. Mundt, C. C. 2002. Use of multiline cultivars and cultivar mixtures for disease management. Annu. Rev. Phytopathol. 40:381-410.
74. Mundt, C. C. 2009. Importance of autoinfection to the epidemiology of polycyclic foliar disease. Phytopathology 99:1116-1120.
75. Mundt, C. C. 2014. Durable resistance: A key to sustainable management of pathogens and pests. Infect. Genet. Evol. 27:446-455.
76. Mundt, C. C., and Leonard, K. J. 1985. A modification of Gregory’s model for describing plant disease gradients. Phytopathology 75:930-935.
77. Mundt, C. C., Leonard, K. J., Thal, W. M., and Fulton, J. H. 1986. 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. Phytopathology 76:590-598.
78. Mundt, C. C., and Sackett, K. E. 2012. Spatial scaling relationships for spread of disease caused by a wind-dispersed plant pathogen. Ecosphere 3:24.
79. Mundt, C. C., Sackett, K. E., and Wallace, L. D. 2011. Landscape heterogeneity and disease spread: experimental approaches with a plant pathogen. Ecol. Appl. 21:321-328.
80. Mundt, C. C., Sackett, K. E., Wallace, L. D., Cowger, C., and Dudley, J. P. 2009a. Long-distance dispersal and accelerating waves of disease: empirical relationships. Am. Nat. 173:456-466.
81. Mundt, C. C., Sackett, K. E., Wallace, L. D., Cowger, C., and Dudley, J. P. 2009b. Aerial dispersal and multiple-scale spread of epidemic disease. EcoHealth 6: 546-552.
82. Mundt, C. C., Wallace, L. D., Allen, T. W., Hollier, C. A., Kemerait, R. C., and Sikora, E. J. 2013. Initial epidemic area is strongly associated with the yearly extent of soybean rust spread in North America. Biol. Invasions 15: 1431-1438.
83. Nathan, R., Klein, E., Robledo-Arnuncio, J. J., and Revilla, E. 2012. Dispersal kernels: Review. Pages 187-210 in: Dispersal Ecology and Evolution. J. Clobert, M. Baguette, T. G. Benton, and J. M. Bullock, eds. Oxford University Press, Oxford, UK.
84. Nathan, R., Perry, G., Cronin, J. T., Strand, A. E., and Cain, M. L. 2003. Methods for estimating long-distance dispersal. Oikos 103:261-273.
85. Newman, M. E. J. 2005. Power laws, Pareto distributions and Zipf’s law. Contemp. Phys. 46:323-351.
86. O’Hara, R. B., and Brown, J. K. M. 1996. Immigration of the barley mildew pathogen into field plots of barley. Plant Pathol. 45:1071-1076.
87. Ojiambo, P. S., Gent, G. H., Mehra, L. K., Christie, D., and Magarey, R. 2017. Focus expansion and stability of the spread parameter estimate of the power law model for dispersal gradients. PeerJ 5:e3465.
88. Papastamati, K., and van den Bosch, F. 2007. The sensitivity of epidemic growth rate to weather variables, with an application to yellow rust on wheat. Phytopathology 97:202-210.
89. Parnell, S., Gottwald, T. R., van den Bosch, F., and Gilligan, C. A. 2009. Optimal strategies for the eradication of Asiatic citrus canker in heterogeneous host landscapes. Phytopathology 99:1370-1376.
90. Peterson, E. K., Hansen, E. M., and Kanaskie, A. 2015. Temporal epidemiology of sudden oak death in Oregon. Phytopathology 105:937-946.
91. Pimentel, D., ed. 2002. Biological invasions: economic and environmental costs of alien plant, animal, and microbe species. CRC Press, Boca Raton, FL.
92. Plantegenest, M., Le May, C., and Fabre, F. 2007. Landscape epidemiology of plant diseases. J. R. Soc. Interface 4:963-972.
93. Pybus, O. G., Suchard, M. A., Lemey, P., Bernardin, F. J., Rambaut, A., Crawford, F. W., Gray, R. R., Arinaminpathy, N., Stramer, S. L., Busch, M. P., and Delwart, E. L. 2012. Unifying the spatial epidemiology and molecular evolution of emerging epidemics. Proc. Natl. Acad. Sci. USA 109:15066-15071.
94. Sackett, K. E., and Mundt, C. C. 2005a. Primary gradients of wheat stripe rust in large field plots. Phytopathology 95:983-991.
95. Sackett, K. E., and Mundt, C. C. 2005b. The effects of dispersal gradient and pathogen life cycle components on epidemic velocity in computer simulations. Phytopathology 95:992-1000.
96. Sackett, K. E., and Mundt, C. C. 2009. Effect of plot geometry on epidemic velocity of wheat yellow rust. Phytopathology 58:370-377.
97. Scherm, H. 1996. On the velocity of epidemic waves in model plant disease epidemics. Ecol. Modell. 87:217-222.
98. Severns, P. M., Estep, L., Sackett, K. E., and Mundt, C. C. 2014. Degree of host susceptibility in the initial disease outbreak influences subsequent epidemic spread. J. Appl. Ecol. 51:1622-1630.
99. Severns, P. M., Sackett, K. E., and Mundt, C. C. 2015. Outbreak propagule pressure influences the landscape spread of a wind-dispersed, epidemic-causing, plant pathogen. Landsc. Ecol. 30:2111-2119.
100. Sexton, A. C., and Howlett, B. J. 2006. Parallels in fungal pathogenesis on plant and animal hosts. Eukaryot. Cell 5:1941-1949.
101. Shaner, G., and Finney, R. E. 1977. The effect of nitrogen fertilization on the expression of slow-mildewing resistance in Knox wheat. Phytopathology 67: 1051-1056.
102. Shaw, M. W., Harwood, T. D., Wilkinson, M. J., and Elliott, L. 2006. Assembling spatially explicit landscape models of pollen and spore dispersal by wind for risk assessment. Proc. R. Soc. Lond., B 273:1705-1713.
103. Shrum, R. 1975. Simulation of wheat stripe rust (Puccinia striiformis West.) using EPIDEMIC, a flexible plant disease simulator. Progress Report 347. Pennsylvania Agricultural Experiment Station, University Park, PA.
104. Simberloff, D. 2009. The role of propagule pressure in biological invasions. Annu. Rev. Ecol. Evol. Syst. 40:81-102.
105. Skellam, J. G. 1951. Random dispersal in theoretical populations. Biometrika 38: 196-218.
106. Stakman, E. C., and Harrar, J. G. 1957. Principles of plant pathology. Ronald, New York.
107. Staskawicz, B. J., Mudgett, M. B., Dangl, J. L., and Galan, J. E. 2001. Common and contrasting themes of plant and animal diseases. Science 292:2285-2289.
108. Tackenberg, O. 2003. Modelling long-distance dispersal of plant diaspores by wind. Ecol. Monogr. 73:173-189.
109. Tatem, A. J., Rogers, D. J., and Hay, S. I. 2006. Global transport networks and infectious disease spread. Adv. Parasitol. 62:293-343.
110. Teng, P. S. 1985. A comparison of simulation approaches to epidemic modeling. Annu. Rev. Phytopathol. 23:351-379.
111. Tildesley, M. J., Bessell, P. R., Keeling, M. J., and Woolhouse, M. E. J. 2009. The role of pre-emptive culling in the control of foot-and-mouth disease. Proc. R. Soc. B 276:3239-3248.
112. Tildesley, M. J., House, T. A., Bruhn, M. C., Curry, R. J., O’Neil, M., Allpress, J. L. E., Smith, G., and Keeling, M. J. 2010. Impact of spatial clustering on disease transmission and optimal control. Proc. Natl. Acad. Sci. USA 107: 1041-1046.
113. Tildesley, M. J., Smith, G., and Keeling, M. J. 2012. Modeling the spread and control of foot-and-mouth disease in Pennsylvania following its discovery and options for control. Prev. Vet. Med. 104:224-239.
114. Tomerlin, J. R., and Howell, T. A. 1988. DISTRAIN: A computer program for training people to estimate disease severity on cereal leaves. Plant Dis. 72: 455-459.
115. Urban, D. L. 2005. Modeling ecological processes across scales. Ecology 86: 1996-2006.
116. van den Bosch, F., Frinking, H. D., Metz, J. A. J., and Zadoks, J. C. 1988a. Focus expansion in plant disease. III: Two experimental examples. Phytopathology 78:919-925.
117. van den Bosch, F., Zadoks, J. C., and Metz, J. A. J. 1988b. Focus expansion in plant disease. I: The constant rate of focus expansion. Phytopathology 78:54-58.
118. van den Bosch, F., Zadoks, J. C., and Metz, J. A. J. 1988c. Focus expansion in plant disease. II. Realistic parameter-sparse models. Phytopathology 78:59-64.
119. van der Plank, J. E. 1963. Plant Diseases: Epidemics and Control. Academic Press, New York.
120. Vespignani, A. 2011. Modelling dynamical processes in complex socio-technical systems. Nat. Phys. 8:32-39.
121. Viswanathan, G. M., Raposo, E. P., and da Luz, M. G. E. 2008. Lévy flights and superdiffusion in the context of biological encounters and random searches. Phys. Life Rev. 5:133-150.
122. Waggoner, P. E. 1962. Weather, space, time, and chance of infection. Phytopathology 52:1100-1108.
123. Waggoner, P. E. 1983. The aerial dispersal of the pathogens of plant disease. Philos. Trans. R. Soc. Lond., B 302:451-462.
124. Wan, A., Zhao, Z., Chen, X., He, Z., Jin, S., Jia, Q., Yao, G., Yang, J., Wang, B., Li, G., Bi, Y., and Yuan, Z. 2004. Wheat stripe rust epidemic and virulence of Puccinia striiformis f. sp. tritici in China in 2002. Plant Dis. 88:896-904.
125. Wang, M. N., Wan, A. M., and Chen, X. M. 2015. Barberry as alternate host is important for Puccinia graminis f. sp. tritici but not for Puccinia striiformis f. sp. tritici in the U.S. Pacific Northwest. Plant Dis. 99:1507-1516.
126. Wellings, C. R. 2007. Puccinia stiiformis in Australia: a review of the incursion, evolution and adaptation of stripe rust in the period 1979-2006. Aust. J. Agric. Res. 58:567-575.
127. WHO Ebola Response Team. 2014. Ebola virus disease in west Africa – the first 9 months of the epidemic and forward projections. N. Engl. J. Med. 371: 1481-1495.
128. Zadoks, J. C., and van den Bosch, F. 1994. On the spread of plant disease: A theory on foci. Annu. Rev. Phytopathol. 32:503-521.
129. Zawolek, M. W., and Zadoks, J. C. 1992. Studies in focus development: An optimum for the dual dispersal of plant pathogens. Phytopathology 82:1288-1297.
130. Zeng, S. M., and Luo, Y. 2008. Systems analysis of wheat stripe rust epidemics in China. Eur. J. Plant Pathol. 121:425-438.