Abstract
Soil baiting was used to monitor temporal and spatial soil inoculum dynamics of Phytophthora cinnamomi in disease centres in four Banksia woodland biomes of the Swan Coastal Plain bioregion and an Eucalyptus marginata forest biome of the Jarrah Forest bioregion of the South-West Botanical Province of Western Australia. Patterns of inoculum occurrence in P. cinnamomi disease centres in Banksia woodland biomes were similar to those in E. marginata forest biomes. Significantly lower frequency of isolation was from near-surface (top 0.03 m) soil and greater occurrence of viable inoculum from soil at depth (∼1 m below the soil surface) and from near-surface soil around the collar of dead Banksia. Seasonal fluctuations in soil inoculum were not as distinct or consistent as that shown for rainfall and temperature and soil water content. Viable inoculum was most frequently isolated from near-surface soil in spring. In all Banksia woodland biomes isolation of inoculum from soil at depth was lowest in summer and greatest in autumn to spring. In all but one biome, isolation of inoculum from soil around dead Banksia was lowest in summer. Inoculum of P. cinnamomi was isolated from groundwater 3-5 m below the soil surface for Banksia woodland biomes in winter and spring 1987 and the winters of 1988 and 1989. Spatial patterns of viable inoculum from soil at depth were aggregated in 42% of quadrats analysed and 34% of quadrats sampled. The pattern of inoculum occurrence found in P. cinnamomi disease centres was influenced by creation of dynamic spatiotemporal niche refuges favourable to the pathogen through ecosystem engineering by host and pathogen.
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References
Beard JS (1984) Biogeography of the Kwongan. In ‘Kwongan plant life of the sandplain’. (Eds JS Pate, JS Beard) pp. 1–26. (University of Western Australia Press: Nedlands)
Beard JS (1989) Definition and location of Banksia woodlands. Journal of the Royal Society of Western Australia 71, 85–86.
Benson DM, Grand LF, Vernia CS, Gottwald TR (2006) Temporal and spatial epidemiology of Phytophthora root rot in Fraser fir plantations. Plant Disease 90, 1171–1180. doi:10.1094/PD-90-1171
Blowes WM, Heather WA, Malajczuk N, Shea SR (1982) The distribution of Phytophthora cinnamomi Rands at two sites in southern Western Australia and at Durras in South-eastern New South Wales. Australian Journal of Botany 30, 139–145. doi:10.1071/BT9820139
Boogert NJ, Paterson DM, Laland KN (2006) The implications of niche construction and ecosystem engineering for conservation biology. Bioscience 56, 570–578. doi:10.1641/0006-3568(2006)56[570:TIONCA] 2.0.CO;2
Burdon JJ, Jarosz AM, Kirby GC (1989) Pattern and patchiness in plantpathogen interactions — causes and consequences. Annual Review of Ecology and Systematics 20, 119–136.
Campbell WA (1951) Vertical distribution of Phytophthora cinnamomi in soil under littleleaf-diseased shortleaf pine. Plant Disease Reporter 35, 26–27.
Campbell CL, Noe JP (1985) The spatial analysis of soilborne pathogens and root diseases. Annual Review of Phytopathology 23, 129–148. doi:10.1146/annurev.py.23.090185.001021
Churchward HM, Dimmock GM (1989) The soils and landforms of the northern jarrah forest. In ‘The jarrah forest. A complex Mediterranean ecosystem’. (Eds B Dell, JJ Havel, N Malajczuk) pp. 13–21. (Kluwer Academic Publishers: Dordrecht)
CoHort Software (2007) ‘CoStat manual. Version 6.’ (CoHort Software: Monterey, CA)
Dell B, Havel JJ (1989) The jarrah forest, an introduction. In ‘The jarrah forest. A complex Mediterranean ecosystem’. (Eds B Dell, JJ Havel, N Malajczuk) pp. 1–10. (Kluwer Academic Publishers: Dordrecht)
Duniway JM (1976) Movement of zoospores of Phytophthora cryptogea in soils of various textures and matric potentials. Phytopathology 66, 877–882. doi:10.1094/Phyto-66-877
Eden MA, Hill RA, Galpoththage M (2000) An efficient baiting assay for quantification of Phytophthora cinnamomi in soil. Plant Pathology 49, 515–522. doi:10.1046/j.1365-3059.2000.00478.x
Franzmann PD, Zappia LR, Patterson BM, Rayner JL, Davis GB (1998) Mineralisation of low concentrations of organic compounds and microbial biomass in surface and vadose zone soils from the Swan Coastal Plain, Western Australia. Australian Journal of Soil Research 36, 921–939. doi:10.1071/S97116
Green RH (1979) ‘Sampling design and statistical methods for environmental biologists.’ (John Wiley & Sons: New York)
Gülser C, Ekberli I (2004) A comparison of estimated and measured diurnal soil temperature through a clay soil depth. Journal of Applied Sciences 4, 418–423. doi:10.3923/jas.2004.418.423
Gupta SC, Larson WE, Allmaras RR (1984) Predicting soil temperature and soil heat flux under different tillage-surface residue conditions. Soil Science Society of America Journal 48, 223–232.
Havel JJ (1975) Site-vegetation mapping in the northern jarrah forest (Darling Range). 1. Definition of site-vegetation types Bulletin 86. Forests Department, Perth.
Hill TCJ, Tippett JT, Shearer BL (1994) Invasion of Bassendean Dune Banksia woodland by Phytophthora cinnamomi. Australian Journal of Botany 42, 725–738. doi:10.1071/BT9940725
Hill TCJ, Tippett JT, Shearer BL (1995) Evaluation of three treatments for eradication of Phytophthora cinnamomi from deep, leached sands in southwest Australia. Plant Disease 79, 122–127. doi:10.1094/PD-79-0122
Holden PA, Fierer N (2005) Microbial processes in the vadose zone. Vadose Zone Journal 4, 1–21. doi:10.2113/4.1.1
Horner IJ, Wilcox WF (1996a) Spatial distribution of Phytophthora cactorum in New York apple orchard soils. Phytopathology 86, 1122–1132. doi:10.1094/Phyto-86-1122
Horner IJ, Wilcox WF (1996b) Temporal changes in activity and dormant spore populations of Phytophthora cactorum in New York apple orchard soils. Phytopathology 86, 1133–1139. doi:10.1094/ Phyto-86-1133
Jacobs KA, MacDonald JD, Berry AM, Costello LR (1997) The effect of low oxygen stress on Phytophthora cinnamomi infection and disease of cork oak roots. In ‘Proceedings of a symposium on oak woodlands: ecology, management and urban interface issues’. General Technical Report PSW-GTR-160. (Eds NH Pillsbury, J Verner, WD Tietje) pp. 553–558. (PSW Research Station, U.S. Department of Agriculture Forest Service: Albany, CA)
Kinal J (1986) Perching and throughflow in a lateritic profile in relation to impact of Phytophthora cinnamomi in the northern jarrah forest. Honours Thesis, Murdoch University, Western Australia.
Kinal J (1993) Soil temperature in the northern jarrah forest in relation to plant and litter cover and implications for the periods and depths at which temperature permit Phytophthora cinnamomi activity. Master of Philosophy Thesis, Murdoch University, Western Australia.
Kinal J, Shearer BL, Fairman RG (1993) Dispersal of Phytophthora cinnamomi through lateritic soil by laterally flowing subsurface water. Plant Disease 77, 1085–1090. doi:10.1094/PD-77-1085
Kirby KN (1993) ‘Advanced data analysis with SYSTAT.’ (Van Nostrad Reinhold: New York)
Larkin RP, Gumpertz ML, Ristaino JB (1995) Geostatistical analysis of Phytophthora epidemic development in commercial bell pepper fields. Phytopathology 85, 191–203. doi:10.1094/Phyto-85-191
Legendre P, Fortin M-J (1989) Spatial pattern and ecological analysis. Vegetatio 80, 107–138. doi:10.1007/BF00048036
Levin SA (1992) The problem of pattern and scale in ecology. Ecology 73, 1943–1967. doi:10.2307/1941447
Levia DF, Frost EE (2006) Variability of throughfall volume and solute inputs in wooded ecosystems. Progress in Physical Geography 30, 605–632. doi:10.1177/0309133306071145
Lewis KJ, Lindgren BS (2000) A conceptual model of biotic disturbance ecology in the central interior of B.C.: how forest management can turn Dr Jekyll into Mr Hyde. Forestry Chronicle 76, 433–443.
Marks GC, Kassaby FY (1974) Detection of Phytophthora cinnamomi in soils. Australian Forestry 36, 198–203.
Marks GC, Kassaby FY, Fagg PC (1975) Variation in population levels of Phytophthora cinnamomi in Eucalyptus forest soils of eastern Victoria. Australian Journal of Botany 23, 435–449. doi:10.1071/ BT9750435
Marshall JK, Chester GW (1992) Effect of forest thinning on jarrah (Eucalyptus marginata) water uptake. Report No. 92/24. CSIRO Division of Water Resources, Floreat Park, Western Australia.
McArthur WM (1991) ‘Reference soils of south-western Australia.’ (Department of Agriculture, Western Australia: Perth)
McLaughlin IM, Jeffers SN (2009) Spatial distribution of Phytophthora cinnamomi in forest soils of the Carolinas. Phytopathology 99, S82.
Miller SA, Madden LV, Schmitthenner AF (1997) Distribution of Phytophthora spp. in field soils determined by immunoassay. Phytopathology 87, 101–107. doi:10.1094/PHYTO.1997.87.1.101
Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100, 403–405. doi:10.1034/j.1600-0706.2003. 12010.x
Murphy DV, Sparling GP, Fillery IRP (1998) Stratification of microbial biomass C and N and gross N mineralisation with soil depth in two contrasting Western Australian agricultural soils. Australian Journal of Soil Research 36, 45–55. doi:10.1071/S97045
Myers N (2001) Mediterranean-climate regions: glowing hotspots of diversity. Journal of Mediterranean Ecology 2, 157–163.
Nulsen RA, Bligh KJ, Baxter IN, Solin EJ, Imrie DH (1986) The fate of rainfall in a mallee and heath vegetated catchment in southern Western Australia. Australian Journal of Ecology 11, 361–371. doi:10.1111/ j.1442-9993.1986.tb01406.x
Otrosina WJ, Marx DH (1975) Populations of Phytophthora cinnamomi and Pythium spp. under shortleaf and loblolly pines in littleleaf disease sites. Phytopathology 65, 1224–1229. doi:10.1094/Phyto-65-1224
Pate JS, Verboom WH, Galloway PD (2001) Co-occurrence of Proteaceae, laterite and related oligotrophic soils: coincidental associations or causative inter-relationships? Australian Journal of Botany 49, 529–560. doi:10.1071/BT00086
Pélissier R, Goreaud F (2001) A practical approach to the study of spatial structure in simple cases of heterogeneous vegetation. Journal of Vegetation Science 12, 99–108. doi:10.2307/3236678
Perry GLW (2004) SpPack: spatial point analysis in Excel using the visual basic for applications (VBA). Environmental Modelling & Software 19, 559–569. doi:10.1016/j.envsoft.2003.07.004
Perry GLW, Enright NJ, Miller BP, Lamont BB (2008) Spatial patterns in species-rich sclerophyll shrublands of southwestern Australia. Journal of Vegetation Science 19, 705–716. doi:10.3170/2008-8-18441
Pressland AJ (1976) Soil moisture redistribution as affected by throughfall and stemflow in an arid zone shrub community. Australian Journal of Botany 24, 641–649. doi:10.1071/BT9760641
Pryce J, Edwards W, Gadek PA (2002) Distribution of Phytophthora cinnamomi at different spatial scales: when can a negative result be considered positively? Austral Ecology 27, 459–462. doi:10.1046/ j.1442-9993.2002.01202.x
Real LA, Biek R (2007) Spatial dynamics and genetics of infectious diseases on heterogeneous landscapes. Journal of the Royal Society, Interface 4, 935–948. doi:10.1098/rsif.2007.1041
Real LA, McElhany P (1996) Spatial pattern and process in plant-pathogen interactions. Ecology 77, 1011–1025. doi:10.2307/2265572
Reddell P, Malajczuk N (1984) Formation of mycorrhizae by jarrah (Eucalyptus marginata Donn ex Smith) in litter and soil. Australian Journal of Botany 32, 511–520. doi:10.1071/BT9840511
Ristaino JB, Gumpertz ML (2000) New frontiers in the study of dispersal and spatial analysis of epidemics caused by species in the genus Phytophthora. Annual Review of Phytopathology 38, 541–576. doi:10.1146/annurev.phyto.38.1.541
Ristaino JB, Larkin RP, Campbell CL (1993) Spatial and temporal dynamics of Phytophthora epidemics in commercial bell pepper fields. Phytopathology 83, 1312–1320. doi:10.1094/Phyto-83-1312
Semeniuk V, Glassford DK (1989) Bassendean and Spearwood Dunes: their geomorphology, stratigraphy and soils as a basis for habitats of Banksia woodlands. Journal of the Royal Society of Western Australia 71, 87–88.
Shea SR, Gillen KJ, Leppard WI (1980) Seasonal variation in population levels of Phytophthora cinnamomi Rands in soil in diseased, freely drained Eucalyptus marginata Sm sites in the northern jarrah forest of south-western Australia. Protection Ecology 2, 135–156.
Shea SR, Shearer B, Tippett J (1982) Recovery of Phytophthora cinnamomi Rands from vertical roots of jarrah (Eucalyptus marginata Sm). Australasian Plant Pathology 11, 25–28. doi:10.1071/APP9820025
Shea SR, Shearer BL, Tippett JT, Deegan PM (1983) Distribution, reproduction, and movement of Phytophthora cinnamomi on sites highly conducive to jarrah dieback in South Western Australia. Plant Disease 67, 970–973. doi:10.1094/PD-67-970
Shearer BL, Dillon M (1995) Susceptibility of plant species in Eucalyptus marginata forest to infection by Phytophthora cinnamomi. Australian Journal of Botany 43, 113–134. doi:10.1071/BT9950113
Shearer BL, Dillon M (1996a) Impact and disease centre characteristics of Phytophthora cinnamomi infestations of Banksia woodlands on the Swan Coastal Plain, Western Australia. Australian Journal of Botany 44, 79–90. doi:10.1071/BT9960079
Shearer BL, Dillon M (1996b) Susceptibility of plant species in Banksia woodlands on the Swan Coastal Plain, Western Australia, to infection by Phytophthora cinnamomi. Australian Journal of Botany 44, 433–445. doi:10.1071/BT9960433
Shearer BL, Fairman RG (2007) Application of phosphite in a high-volume foliar spray delays and reduces the rate of mortality of four Banksia species infected with Phytophthora cinnamomi. Australasian Plant Pathology 36, 358–368. doi:10.1071/AP07033
Shearer BL, Hill TC (1989) Diseases of Banksia woodlands on the Bassendean and Spearwood Dune Systems. Journal of the Royal Society of Western Australia 71, 113–114.
Shearer BL, Shea SR (1987) Variation in seasonal population fluctuations of Phytophthora cinnamomi within and between infected Eucalyptus marginata sites of southwestern Australia. Forest Ecology and Management 21, 209–230. doi:10.1016/0378-1127(87)90044-2
Shearer BL, Smith IW (2000) Disease of eucalypts caused by soilborne species of Phytophthora and Pythium. In ‘Diseases and pathogens of Eucalypts’. (Eds PJ Keane, GA Kile, FD Podger, BN Brown) pp. 259–291. (CSIRO Publishing: Melbourne)
Shearer BL, Tippett JT (1989) Jarrah dieback: the dynamics and management of Phytophthora cinnamomi in the jarrah (Eucalyptus marginata) forest of south-western Australia. Research Bulletin 3. Department of Conservation and Land Management, Perth.
Shearer BL, Shea SR, Deegan PM (1987) Temperature-growth relationships of Phytophthora cinnamomi in the secondary phloem of roots of Banksia grandis and Eucalyptus marginata. Phytopathology 77, 661–665. doi:10.1094/Phyto-77-661
Shearer BL, Crane CE, Cochrane A (2004) Quantification of the susceptibility of the native flora of the South-West Botanical Province, Western Australia, to Phytophthora cinnamomi. Australian Journal of Botany 52, 435–443. doi:10.1071/BT03131
Shearer BL, Crane CE, Barrett S, Cochrane A (2007) Phytophthora cinnamomi invasion, a major threatening process to conservation of flora diversity in the South-west Botanical Province of Western Australia. Australian Journal of Botany 55, 225–238. doi:10.1071/ BT06019
Shearer BL, Crane CE, Fairman RG, Dunne CP (2009) Ecosystem dynamics altered by pathogen-mediated changes following invasion of Banksia woodland and Eucalyptus marginata forest biomes of south-western Australia by Phytophthora cinnamomi. Australasian Plant Pathology 38, 417–436. doi:10.1071/AP09018
Specht RL (1957) Dark Island Heath (Ninety-Mile Plain, South Australia). IV. Soil moisture patterns produced by rainfall interception and stemflow. Australian Journal of Botany 5, 137–150. doi:10.1071/BT9570137
Stoneman GL, Dell B, Turner NC (1995) Growth of Eucalyptus marginata (jarrah) seedlings in mediterranean-climate forest in south-west Australia in response to overstorey, site and fertiliser application. Forest Ecology and Management 79, 173–184. doi:10.1016/0378-1127(95)03608-3
Taylor WA (2000) Change-point analysis: a powerful new tool for detecting change. Available at http://www.variation.com/cpa/tech/changepoint. html [Verified 23 February 2010]
Taylor WA (2008) Change-point analyzer software. Available at http:// www.variation.com/cpa/index.html [Verified 23 February 2010]
ba]Tsao PH (1983) Factors affecting isolation and quantification of Phytophthora from soil. In ‘Phytophthora. Its biology, taxonomy, ecology and pathology’. (Eds DC Erwin, S Bartnicki-Garcia, PH Tsao) pp. 219–236. (The American Phytopathological Society: St Paul, MN)
Tsao PH, Guy SO (1977) Inhibition of Mortierella and Pythium in a Phytophthora-isolation medium containing hymexazol. Phytopathology 67, 796–801. doi:10.1094/Phyto-67-796
Verboom WH, Pate JS (2006) Bioengineering of soil profiles in semiarid ecosystems: the ‘phytotarium’ concept. A review. Plant and Soil 289, 71–102. doi:10.1007/s11104-006-9073-8
Weste G (2003) The dieback cycle in Victorian forests: a 30-year study of changes caused by Phytophthora cinnamomi in Victorian open forests, woodlands and heathlands. Australasian Plant Pathology 32, 247–256. doi:10.1071/AP03013
Weste G, Ruppin P (1977) Phytophthora cinnamomi: population densities in forest soils. Australian Journal of Botany 25, 461–475. doi:10.1071/ BT9770461
Weste G, Walchhuetter T, Walshe T (1999) Regeneration of Xanthorrhoea australis following epidemic disease due to Phytophthora cinnamomi in the Brisbane Ranges, Victoria. Australasian Plant Pathology 28, 162–169. doi:10.1071/AP99027
Workneh F, Yang XB, Tylka GL (1998) Effect of tillage practices on vertical distribution of Phytophthora sojae. Plant Disease 82, 1258–1263. doi:10.1094/PDIS.1998.82.11.1258
Zak B (1961) Aeration and other soil factors affecting southern pines as related to littleleaf disease. Southern Forest Experiment Station Technical Bulletin 1248. U.S. Government Printing Office, Washington, DC.
Zentmyer GA (1980) ‘Phytophthora cinnamomi and the diseases it causes.’ Monograph 10. (The American Phytopathological Society: St Paul, MN)
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Shearer, B.L., Dillon, M.J., Kinal, J. et al. Temporal and spatial soil inoculum dynamics following Phytophthora cinnamomi invasion of Banksia woodland and Eucalyptus marginata forest biomes of south-western Australia. Australasian Plant Pathol. 39, 293–311 (2010). https://doi.org/10.1071/AP09095
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DOI: https://doi.org/10.1071/AP09095