Effects of individual, community, and landscape drivers on the dynamics of a wildland forest epidemic

Ecology

Volumn 97, Issue 3, 2016, Pages 649-660

  Haas, Sarah E ^a,d   Cushman, J Hall ^b   Dillon, Whalen W ^a   Rank, Nathan E ^b   Rizzo, David M ^c   Meentemeyer, Ross K ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b SONOMA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d TEXAS PARKS AND WILDLIFE DEPARTMENT   (United States)

Author keywords

Diversity disease risk; Emerging infectious disease; Landscape epidemiology; Pathogen spillover; Phytophthora ramorum; Seasonality; Sudden oak death; Survival analysis; Time varying covariate

Indexed keywords

ANNUAL VARIATION; COMMUNITY STRUCTURE; DISEASE PREVALENCE; DISEASE TRANSMISSION; EPIDEMIC; FOREST ECOSYSTEM; HETEROGENEITY; HOST-PATHOGEN INTERACTION; INFECTIOUS DISEASE; LANDSCAPE ECOLOGY; RISK FACTOR; SEASONALITY; SHRUB; SPECIES RICHNESS; SURVIVAL;

CALIFORNIA; UNITED STATES;

LAURUS NOBILIS; PHYTOPHTHORA RAMORUM; QUERCUS; QUERCUS AGRIFOLIA; QUERCUS CHRYSOLEPIS; QUERCUS VELUTINA; UMBELLULARIA CALIFORNICA;

CALIFORNIA; FOREST; MICROBIOLOGY; OAK; PHYSIOLOGY; PHYTOPHTHORA; PLANT DISEASE; TIME FACTOR;

CALIFORNIA; FORESTS; PHYTOPHTHORA; PLANT DISEASES; QUERCUS; TIME FACTORS;

EID: 84962091337     PISSN: 00129658     EISSN: 19399170     Source Type: Journal    
DOI: 10.1890/15-0767     Document Type: Article

References (82)

1. Alexander, H. M. 2010. Disease in natural plant populations, communities, and ecosystems: insights into ecological and evolutionary processes. Plant Disease 94:492-503.
2. Altizer, S., A. Dobson, P. Hosseini, P. Hudson, M. Pascual, and P. Rohani. 2006. Seasonality and the dynamics of infectious diseases. Ecology Letters 9:467-484.
3. Anacker, B. L., N. E. Rank, D. Huberli, M. Garbelotto, S. Gordon, T. Harnik, R. Whitkus, and R. K. Meentemeyer. 2007. Susceptibility to Phytophthora ramorum in a key infectious host: landscape variation in host genotype, host phenotype, and environmental factors. New Phytologist 177:756-766.
4. Aukema, J. E., D. G. McCullough, B. Von Holle, A. M. Liebhold, K. Britton, and S. J. Frankel. 2010. Historical accumulation of nonindigenous forest pests in the continental United States. BioScience 60:886-897.
5. Beckstead, J., S. E. Meyer, B. M. Connolly, M. B. Huck, and L. E. Street. 2010. Cheatgrass facilitates spillover of a seed bank pathogen onto native grass species. Journal of Ecology 98:168-177.
6. Bell, D., J. Bradford, and W. Lauenroth. 2015. Scale dependence of disease impacts on quaking aspen (Populus tremuloides) mortality in the southwestern United States. Ecology 96:1835-1845.
7. Brasier, C. M., and J. Webber. 2010. Sudden larch death. Nature 466:824-825.
8. Brown, L. B., and B. Allen-Diaz. 2009. Forest stand dynamics and sudden oak death: mortality in mixed-evergreen forests dominated by coast live oak. Forest Ecology and Management 257:1271-1280.
9. Burdon, J. J., and G. A. Chilvers. 1982. Host density as a factor in plant disease ecology. Annual Review of Phytopathology 20:143-166.
10. Chambers, J. M., W. S. Cleveland, B. Kleiner, and P. A. Tukey. 1983. Graphical methods for data analysis. Wadsworth International Group, Belmont, California, USA.
11. Cobb, R. C., R. K. Meentemeyer, and D. M. Rizzo. 2010. Apparent competition in canopy trees determined by pathogen transmission rather than susceptibility. Ecology 91:327-333.
12. Cobb, R. C., J. A. N. Filipe, R. K. Meentemeyer, C. A. Gilligan, and D. M. Rizzo. 2012. Ecosystem transformation by emerging infectious disease: loss of large tanoak from California forests. Journal of Ecology 100:712-722.
13. Condeso, T. E., and R. K. Meentemeyer. 2007. Effects of landscape heterogeneity on the emerging forest disease sudden oak death. Journal of Ecology 95:364-375.
14. Cronin, J., M. Welsh, M. Dekkers, S. Abercrombie, and C. E. Mitchell. 2010. Host physiological phenotype explains pathogen reservoir potential. Ecology Letters 13:1221-1232.
15. Cushman, J. H., and R. K. Meentemeyer. 2008. Multi-scale patterns of human activity and the incidence of an exotic forest pathogen. Journal of Ecology 96:766-776.
16. Davidson, J. M., A. C. Wickland, H. A. Patterson, K. R. Falk, and D. M. Rizzo. 2005. Transmission of Phytophthora ramorum in mixed-evergreen forest in California. Phytopathology 95:587-596.
17. Davidson, J. M., H. A. Patterson, and D. M. Rizzo. 2008. Sources of inoculum for Phytophthora ramorum in a redwood forest. Phytopathology 98:860-866.
18. Davidson, J. M., H. A. Patterson, A. C. Wickland, E. J. Fichtner, and D. M. Rizzo. 2011. Forest type influences transmission of Phytophthora ramorum in California oak woodlands. Phytopathology 101:492-501.
19. Desprez-Loustau, M., C. Robin, G. Reynaud, M. Deque, V. Badeau, D. Piou, C. Husson, and B. Marcais. 2007. Simulating the effects of a climate-change scenario on the geographical range and activity of forest-pathogenic fungi. Canadian Journal of Plant Pathology 29:101-120.
20. DiLeo, M. V., R. M. Bostock, and D. M. Rizzo. 2014. Microclimate impacts survival and prevalence of Phytophthora ramorum in Umbellularia californica, a key reservoir host of sudden oak death in Northern California forests. PLoS ONE 9:1-6.
21. Dillon, W. W., S. E. Haas, D. M. Rizzo, and R. K. Meentemeyer. 2014. Perspectives of spatial scale in a wildland forest epidemic. European Journal of Plant Pathology 138:449-465.
22. Dukes, J. S., et al. 2009. Responses of insect pests, pathogens, and invasive plant species to climate change in the forests of northeastern North America: what can we predict? Canadian Journal of Forest Research 39:231-248.
23. Ellis, A. M., T. Vaclavik, and R. K. Meentemeyer. 2010. When is connectivity important? A case study of the spatial pattern of sudden oak death. Oikos 119:485-493.
24. Ellison, A. M., et al. 2005. Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment 3:479-486.
25. Eyre, C. A., M. Kozanitas, and M. Garbelotto. 2013. Population dynamics of aerial and terrestrial populations of Phytophthora ramorum in a California forest under different climatic conditions. Phytopathology 103:1141-1152.
26. Fisher, M. C., D. A. Henk, C. J. Briggs, J. S. Brownstein, L. C. Madoff, S. L. McCraw, and S. J. Gurr. 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186-194.
27. Freckleton, R. P., and O. T. Lewis. 2006. Pathogens, density dependence and the coexistence of tropical trees. Proceedings of the Royal Society B 273:2909-2916.
28. Garrett, K., L. Zuniga, E. Roncal, G. Forbes, C. Mundt, Z. Su, and R. Nelson. 2009. Intraspecific functional diversity in hosts and its effect on disease risk across a climatic gradient. Ecological Applications 19:1868-1883.
29. Haas, S. E., M. B. Hooten, D. M. Rizzo, and R. K. Meentemeyer. 2011. Forest species diversity reduces disease risk in a generalist plant pathogen invasion. Ecology Letters 14:1108-1116.
30. Haavik, L. J., and F. M. Stephen. 2010. Stand and individual tree characteristics associated with Enaphalodes rufulus (Haldeman) (Coleoptera: Cerambycidae) infestations within the Ozark and Ouachita National Forests. Forest Ecology and Management 259:1938-1945.
31. Hantsch, L., U. Braun, M. Scherer-Lorenzen, and H. Bruelheide. 2013. Species richness and species identity effects on occurrence of foliar fungal pathogens in a tree diversity experiment. Ecosphere 4:1-12.
32. Hatala, J. A., M. C. Dietze, R. L. Crabtree, K. Kendall, D. Six, and P. R. Moorcroft. 2011. An ecosystem-scale model for the spread of a host-specific forest pathogen in the Greater Yellowstone Ecosystem. Ecological Applications 21:1138-1153.
33. Hawley, D. M., and S. M. Altizer. 2011. Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Functional Ecology 25:48-60.
34. Hohl, A., T. Václavík, and R. K. Meentemeyer. 2013. Go with the flow: geospatial analytics to quantify hydrologic landscape connectivity for passively dispersed microorganisms. International Journal of Geographical Information Science 28:1626-1641.
35. Holdenrieder, O., M. Pautasso, P. J. Weisberg, and D. Lonsdale. 2004. Tree diseases and landscape processes: the challenge of landscape pathology. Trends in Ecology and Evolution 19:446-452.
36. Jacobi, W., B. Geils, J. Taylor, and W. Zentz. 1993. Predicting the incidence of comandra blister rust on lodgepole pine: site, stand, and alternate-host influences. Phytopathology 83:630-637.
37. Jones, R. A. C. 2009. Plant virus emergence and evolution: origins, new encounter scenarios, factors driving emergence, effects of changing world conditions, and prospects for control. Virus Research 141:113-130.
38. Jules, E. S., A. L. Carroll, A. M. Garcia, C. M. Steenbock, and M. J. Kauffman. 2014. Host heterogeneity influences the impact of a non-native disease invasion on populations of a foundation tree species. Ecosphere 5:1-17.
39. Kanaskie, A., E. Goheen, N. Osterbauer, M. McWilliams, E. Hansen, and W. Sutton 2008. Eradication of Phytophthora ramorum from Oregon forests: status after six years. Pages 15-17 in S. J. Frankel, J. T. Kliejunas, and K. Palmieri, editors. Proceedings of the sudden oak death third science symposium. Pacific Southwest Research Station, U.S. Department of Agriculture, Forest Service, Albany, California, USA.
40. Kauffman, M., and E. S. Jules. 2006. Heterogeneity shapes invasion: host size and environment influence susceptibility to a nonnative pathogen. Ecological Applications 16:166-175.
41. Keesing, F., et al. 2010. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647-652.
42. Keesing, F., R. D. Holt, and R. S. Ostfeld. 2006. Effects of species diversity on disease risk. Ecology Letters 9:485-498.
43. Kleinbaum, D. G., and M. Klein. 2012. Survival analysis: a self-learning text, Third edition. Springer, New York, New York, USA.
44. Kliejunas, J. 2010. Sudden oak death and Phytophthora ramorum: a summary of the literature. 2010 edition. General Technical Report PSW-GTR-234. U.S. Department of Agriculture, Forest Service, Pacific Southwest Research Station, Albany California, USA.
45. Kliejunas, J. T. 2011. A risk assessment of climate change and the impact of forest diseases on forest ecosystems in the Western United States and Canada. General Technical Report PSW-GTR-236. U.S. Department of Agriculture, Forest Service, Pacific Southwest Research Station, Albany, California, USA.
46. Kovacs, K., T. Vaclavik, R. G. Haight, A. Pang, N. J. Cunniffe, C. A. Gilligan, and R. K. Meentemeyer. 2011. Predicting the economic costs and property value losses attributed to sudden oak death damage in California (2010-2020). Journal of Environmental Management 92:1292-1302.
47. Kueh, K. H., S. F. McKay, E. Facelli, J. M. Facelli, R. M. A. Velzeboer, A. J. Able, and E. S. Scott. 2012. Response of selected South Australian native plant species to Phytophthora cinnamomi. Plant Pathology 61:1165-1178.
48. Lamsal, S., R. C. Cobb, J. H. Cushman, Q. M. Meng, D. M. Rizzo, and R. Meentemeyer. 2011. Spatial estimation of the density and carbon content of host populations for Phytophthora ramorum in California and Oregon. Forest Ecology and Management 262:989-998.
49. Larson, E. R. 2011. Influences of the biophysical environment on blister rust and mountain pine beetle, and their interactions, in whitebark pine forests. Journal of Biogeography 38:453-470.
50. Lloyd-Smith, J. O., S. J. Schreiber, P. E. Kopp, and W. M. Getz. 2005. Superspreading and the effect of individual variation on disease emergence. Nature 438:355-359.
51. Lovett, G. M., C. D. Canham, M. A. Arthur, K. C. Weathers, and R. D. Fitzhugh. 2006. Forest ecosystem responses to exotic pests and pathogens in eastern North America. BioScience 56:395-405.
52. McPherson, B. A., S. R. Mori, D. L. Wood, A. J. Storer, P. Svihra, M. Kelly, and R. B. Standiford. 2005. Sudden oak death in California: disease progression in oak and tanoaks. Forest Ecology and Management 213:71-89.
53. McPherson, B. A., S. R. Mori, D. L. Wood, M. Kelly, A. J. Storer, P. Svihra, and R. B. Standiford. 2010. Responses of oaks and tanoaks to the sudden oak death pathogen after 8 yr of monitoring in two coastal California forests. Forest Ecology and Management 259:2248-2255.
54. Meentemeyer, R. K., N. E. Rank, B. L. Anacker, D. M. Rizzo, and J. H. Cushman. 2008a. Influence of land-cover change on the spread of an invasive forest pathogen. Ecological Applications 18:159-171.
55. Meentemeyer, R. K., N. E. Rank, D. A. Shoemaker, C. B. Oneal, A. C. Wickland, K. M. Frangioso, and D. M. Rizzo. 2008b. Impact of sudden oak death on tree mortality in the Big Sur ecoregion of California. Biological Invasions 10:1243-1255.
56. Meentemeyer, R. K., N. J. Cunniffe, A. R. Cook, J. A. N. Filipe, R. D. Hunter, D. M. Rizzo, and C. A. Gilligan. 2011. Epidemiological modeling of invasion in heterogeneous landscapes: spread of sudden oak death in California (1990-2030). Ecosphere 2:art17.
57. Meentemeyer, R. K., S. E. Haas, and T. Vaclavik. 2012. Landscape epidemiology of emerging infectious diseases in natural and human-altered ecosystems. Annual Review of Phytopathology 50:379-402.
58. Metz, M., K. M. Frangioso, A. C. Wickland, and R. K. Meentemeyer. 2012. An emergent disease causes directional changes in forest species composition in coastal California. Ecosphere 3:art86.
59. Mitchell, C. E., D. Tilman, and J. V. Groth. 2002. Effects of grassland plant species diversity, abundance, and composition on foliar fungal disease. Ecology 83:1713-1726.
60. Moore, S., and E. Borer. 2012. The influence of host diversity and composition on epidemiological patterns at multiple spatial scales. Ecology 93:1095-1105.
61. Mordecai, E. A. 2011. Pathogen impacts on plant communities: unifying theory, concepts, and empirical work. Ecological Monographs 81:429-441.
62. Ostfeld, R. S., and F. Keesing. 2000. Biodiversity and disease risk: the case of Lyme disease. Conservation Biology 14:722-728.
63. Ostfeld, R. S., and F. Keesing. 2012. Effects of host diversity on infectious disease. Annual Review of Ecology, Evolution, and Systematics 43:157-161.
64. Paillet, F. L. 2002. Chestnut: history and ecology of a transformed species. Journal of Biogeography 29:1517-1530.
65. Perkins, T. E., and G. R. Matlack. 2002. Human-generated pattern in commercial forests of southern Mississippi and consequences for the spread of pests and pathogens. Forest Ecology and Management 157:143-154.
66. Pimentel, D., R. Zuniga, and D. Morrison. 2005. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52:273-288.
67. Power, A. G., and C. E. Mitchell. 2004. Pathogen spillover in disease epidemics. American Naturalist 164:S79-S89.
68. Preisler, H. K., J. A. Hicke, A. A. Ager, and J. L. Hayes. 2012. Climate and weather influences on spatial temporal patterns of mountain pine beetle populations in Washington and Oregon. Ecology 93:2421-2434.
69. R Development Core Team. 2010. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. www.R-Project.org
70. Rizzo, D. M., and M. Garbelotto. 2003. Sudden oak death: endangering California and Oregon forest ecosystems. Frontiers in Ecology and the Environment 1:197-204.
71. Rizzo, D. M., M. Garbelotto, J. M. Davidson, G. W. Slaughter, and S. T. Koike. 2002. Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densiflorus in California. Plant Disease 86:205-214.
72. Rizzo, D. M., M. Garbelotto, and E. M. Hansen. 2005. Phytophthora ramorum: integrative research and management of an emerging pathogen in California and Oregon forests. Annual Review of Phytopathology 43:309-335.
73. Rondeau, V., L. Filleul, and P. Joly. 2006. Nested frailty models using maximum penalized likelihood estimation. Statistics in Medicine 25:4036-4052.
74. Rondeau, V., Y. Mazroui, and J. R. Gonzalez. 2012. frailtypack: an R package for the analysis of correlated survival data with frailty models using penalized likelihood estimation or parametrical estimation. Journal of Statistical Software 47:1-28.
75. Smith, J. P., and J. T. Hoffman. 2001. Site and stand characteristics related to white pine blister rust in high-elevation forests of Southern Idaho and Western Wyoming. Western North American Naturalist 61:409-416.
76. Sturrock, R. N., S. J. Frankel, A. V. Brown, P. E. Hennon, J. T. Kliejunas, K. J. Lewis, J. J. Worrall, and a. J. Woods. 2011. Climate change and forest diseases. Plant Pathology 60:133-149.
77. Sullivan, L. L., B. L. Johnson, L. A. Brudvig, and N. M. Haddad. 2011. Can dispersal mode predict corridor effects on plant parasites? Ecology 92:1559-1564.
78. Swiecki, T. J., and E. Bernhardt 2006. Disease risk factors and disease progress in coast live oak and tanoak affected by Phytophthora ramorum canker (sudden oak death). Pages 383-411 in S. J. Frankel, P. J. Shea, and M. I. Haverty, editors. Proceedings of the sudden oak death second science symposium: the state of our knowledge. Pacific Southwest Research Station, U.S. Department of Agriculture, Forest Service, Albany, California, USA.
79. Swiecki, T. J., and E. Bernhardt 2010. Long-term trends in coast live oak and tanoak stands affected by Phytophthora ramorum canker (sudden oak death). Pages 207-209 in S. J. Frankel, J. T. Kliejunas, and K. Palmieri, editors. Proceedings of the sudden oak death fourth science symposium. Pacific Southwest Research Station, U.S. Department of Agriculture, Forest Service, Albany, California, USA.
80. Swiecki, T. J., and E. A. Bernhardt 2013. A reference manual for managing sudden oak death in California. General Technical Report PSW-GTR-242. U.S. Department of Agriculture, Forest Service, Pacific Southwest Research Station, Albany, California, USA.
81. Therneau, T. 2014.coxme: mixed effects cox models. R package version 2.2-3. http://CRAN.R-project.org/package=coxme
82. Wickland, A. C., C. E. Jensen, and D. M. Rizzo. 2008. Geographic distribution, disease symptoms and pathogenicity of Phytophthora nemorosa and Phytophthora pseudosyringae in California, USA. Forest Pathology 38:288-298.