Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Phytophthora cinnamomi invasion, a major threatening process to conservation of flora diversity in the South-west Botanical Province of Western Australia

B. L. Shearer A C , C. E. Crane A , S. Barrett B and A. Cochrane A
+ Author Affiliations
- Author Affiliations

A Science Division, Department of Environment and Conservation, Locked Bag 104, Bentley Delivery Centre, WA 6983, Australia.

B South Coast Region, Department of Environment and Conservation, Albany, WA 6330, Australia.

C Corresponding author: Email: Bryan.Shearer@dec.wa.gov.au

Australian Journal of Botany 55(3) 225-238 https://doi.org/10.1071/BT06019
Submitted: 3 February 2006  Accepted: 28 November 2006   Published: 18 May 2007

Abstract

The invasive soilborne plant pathogen Phytophthora cinnamomi Rands is a major threatening process in the South-west Botanical Province of Western Australia, an internationally recognised biodiversity hotspot. Comparatively recent introduction of P. cinnamomi into native plant communities of the South-west Botanical Province of Western Australia since the early 1900s has caused great irreversible damage and altered successional change to a wide range of unique, diverse and mainly susceptible plant communities. The cost of P. cinnamomi infestation to community values is illustrated by examination of direct (mortality curves, changes in vegetation cover) and indirect impacts on biodiversity and ecosystem dynamics, the proportion of Threatened Ecological Communities infested, Declared Rare Flora either directly or indirectly threatened by infestation and estimates of the proportion of the native flora of the South-west Botanical Province susceptible to the pathogen. While direct impacts of P. cinnamomi have been poorly documented in the South-west Botanical Province, even less attention has been given to indirect impact where destruction of the habitat by the pathogen affects taxa not directly affected by infection. Current poor understanding and quantification of indirect impacts of P. cinnamomi through habitat destruction results in an underestimation of the true impact of the pathogen on the flora of the South-west Botanical Province. Considerable variation of susceptibility to P. cinnamomi among and within families of threatened flora and responses of taxa within the genus Lambertia show how classification within family and genus are poor predictors of species susceptibility. Within apparently susceptible plant species, individuals are resistant to P. cinnamomi infection. Intra-specific variation in susceptibility can be utilised in the long-term management of threatened flora populations and needs to be a high research priority. Current control strategies for conservation of flora threatened by P. cinnamomi integrate hygiene and ex situ conservation with disease control using fungicide. Application of the fungicide phosphite has proven effective in slowing progress of P. cinnamomi in infested, threatened communities. However, variation in plant species responses to phosphite application is a major factor influencing effective control of P. cinnamomi in native communities. A greater understanding of the mechanisms of action of phosphite in plant species showing different responses to the fungicide may provide options for prescription modification to increase phosphite effectiveness in a range of plant species. The range of responses to P. cinnamomi infection and phosphite application described for Lambertia taxa suggests that the genus would make an ideal model system to elucidate the mechanisms of resistance to P. cinnamomi and the effectiveness of phosphite against the pathogen.


Acknowledgements

Our thanks go to A. Crawford for germinating seed, V. English and J. Pryde for help in compiling Table 4, E. Adams, R. Carter, V. Clarke, M. Garkakalis, R. Hearn, B. Loudon, C. Page, N. Rouse, R. Smith and M. Streilein for help in compiling Table 5, R. Fairman for help with impact assessments, and C. Dunne and M. Shearer for checking the manuscript.


References


Barker PCJ, Wardlaw TJ (1995) Susceptibility of selected Tasmanian rare plants to Phytophthora cinnamomi. Australian Journal of Botany 43, 379–386.
Crossref | GoogleScholarGoogle Scholar | open url image1

Barrett S (2003) Monitoring of aerial phosphite applications for the control of Phytophthora cinnamomi in the Albany district. In ‘Phytophthora in forests and natural ecosystems’. 2nd international IUFRO working party 7.02.09 meeting, Albany, WA. (Eds JA McComb, GEStJ Hardy, IC Tommerup) pp. 132–137. (Murdoch University Print: Perth)

Barrett SR, Shearer BL, Hardy GEStJ (2003) The efficacy of phosphite applied after inoculation on the colonisation of Banksia brownii stems by Phytophthora cinnamomi. Australasian Plant Pathology 32, 1–7.
Crossref | GoogleScholarGoogle Scholar | open url image1

Butcher TB, Stukely MJC, Chester GW (1984) Genetic variation in resistance of Pinus radiata to Phytophthora cinnamomi. Forest Ecology and Management 8, 197–220.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cho JJ (1983) Variability in susceptibility of some Banksia species to Phytophthora cinnamomi and their distribution in Australia. Plant Disease 67, 869–871. open url image1

Coates DJ (2000) Defining conservation units in a rich and fragmented flora: implications for the management of genetic resources and evolutionary processes in south-west Australian plants. Australian Journal of Botany 48, 329–339.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cochrane A, Coates D (1994) Western Australia’s Threatened Flora Seed Centre and its role in conservation of genetic diversity. Danthonia 3, 4–7. open url image1

Commonwealth of Australia (2005) ‘Environment Protection and Biodiversity Conservation Act 1999.’ (Commonwealth Government Printer: Canberra)

Davison EM, Shearer BL (1989) Phytophthora spp. in indigenous forests in Australia. New Zealand Journal of Forestry Science 19, 277–289. open url image1

Dixon KW, Thinlay , Sivasithamparam K (1984) Technique for rapid assessment of tolerance of Banksia spp. to root rot caused by Phytophthora cinnamomi. Plant Disease 68, 1077–1080. open url image1

Dobrowolski MP, Tommerup IC, Shearer BL, O’Brien PA (2003) Three clonal lineages of Phytophthora cinnamomi in Australia revealed by microsatellites. Phytopathology 93, 695–704.
Crossref |
open url image1

D’Souza NK, Colqhhoun IJ, Shearer BL, Hardy GEStJ (2004) The potential of five Western Australian native Acacia species for biological control of Phytophthora cinnamomi. Australian Journal of Botany 52, 267–279.
Crossref | GoogleScholarGoogle Scholar | open url image1

D’Souza NK, Colqhhoun IJ, Shearer BL, Hardy GEStJ (2005) Assessing the potential for biological control of Phytophthora cinnamomi by fifteen native Western Australian jarrah-forest legume species. Australasian Plant Pathology 34, 533–540.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dudzinski MJ, Old KM, Gibbs RJ (1993) Pathogenic variability in Australian isolates of Phytophthora cinnamomi. Australian Journal of Botany 41, 721–732.
Crossref | GoogleScholarGoogle Scholar | open url image1

Englander L, Merlino JA, McGuire JJ (1980) Efficacy of two new systemic fungicides and ethazole for control of phytophthora root rot of rhododendron, and spread of Phytophthora cinnamomi in propagation benches. Phytopathology 70, 1175–1179. open url image1

Frampton J, Benson DM (2004) Phytophthora root rot mortality in fraser fir seedlings. HortScience 39, 1025–1026. open url image1

Frazer GW , Canham CD , Letzman KP (1999) ‘Gap light analyser (GLA): imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs. Users manual and program documentation, Version 2.0.’ (Simon Frazer University: Burnaby, British Columbia; and the Institute of Ecosystem Studies: Millbrook, New York)

Grant M , Barrett S (2003) The distribution and impact of Phytophthora cinnamomi Rands in the south coast region of Western Australia. In ‘Phytophthora in forests and natural ecosystems’. 2nd international IUFRO working party 7.02.09 meeting, Albany, WA. (Eds JA McComb, GEStJ Hardy, IC Tommerup) pp. 34–40. (Murdoch University Print: Perth)

Guest D, Grant B (1991) The complex action of phosphonates as antifungal agents. Biological Review 66, 159–187. open url image1

Hansen EM (1999) Disease and diversity in forest ecosystems. Australasian Plant Pathology 28, 313–319.
Crossref | GoogleScholarGoogle Scholar | open url image1

Harris JA, Kassaby FY, Smith IW (1985) Variations in mortality in families of Eucalyptus regnans caused by Phytophthora cinnamomi up to 5 years after planting. Australian Forest Research 15, 57–65. open url image1

Havel JJ (1975) Site-vegetation mapping in the northern jarrah forest (Darling Range). 1. Definition of site-vegetation types Bulletin 86. Forests Departmenty, Perth.

Hill TCJ, Tippett JT, Shearer BL (1994) Invasion of Bassendean Dune Banksia woodland by Phytophthora cinnamomi. Australian Journal of Botany 42, 725–738.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hobbs RJ, Arico S, Aronson J, Baron JS, Bridgewater P, Cramer VA, Epstein PR, Ewel JJ, Klink CA, Lugo AE, Norton D, Ojima D, Richardson DM, Sanderson EW, Valladares F, Vilà M, Zamora R, Zobel M (2006) Novel ecosystems: theoretical and management aspects of the new ecological world order. Global Ecology and Biogeography 15, 1–7.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hope PK, Drosdowsky W, Nicholls N (2006) Shifts in the synoptic systems influencing southwest Western Australian. Climate Dynamics 26, 751–764.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hopkins ER (1973) Crown dieback in eucalypt forest. In ‘Eucalypt dieback in Australia’. Proceedings of the Lakes Entrance seminar. (Eds GC Marks, RM Idczak) pp.1–16. (Forests Commission: Melbourne)

Hopper SD, Gioia P (2004) The southwest Australian floristic region: evolution and conservation of a global hot spot of biodiversity. Annual Review of Ecology and Evolutionary Systematics 35, 623–650.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hnatiuk RJ (1995) 40. Lambertia. In ‘Flora of Australia. Volume 16, Elaeagraceae, Proteaceae 1’. pp. 425–436. (CSIRO Publishing: Melbourne)

Hüberli D, Tommerup IC, Calver MC, Colqhhoun IJ, Hardy GEStJ (2002) Temperature and inoculation method influence disease phenotypes and mortality of Eucalyptus marginata clonal lines inoculated with Phytophthora cinnamomi. Australasian Plant Pathology 31, 107–118.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jennings SB, Brown ND, Sheil D (1999) Assessing forest canopies and understorey illumination: canopy closure, canopy cover and other measures. Forestry 72, 59–73.
Crossref | GoogleScholarGoogle Scholar | open url image1

Keighery GJ (1983) New species from the Stirling Range of Western Australia. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 104, 177–182. open url image1

Keighery GJ, Coates DJ, Gibson N (1994) Future ecosystems—ecological balance (ecological impact of disease causing fungi in south-western Australia). Journal of the Royal Society of Western Australia 77, 181–184. open url image1

Kenerley CM, Bruck RI (1987) Distribution and disease progress of phytophthora root rot of fraser fir seedlings. Phytopathology 77, 520–526. open url image1

Kennedy J, Weste G (1986) Vegetation changes associated with invasion by Phytophthora cinnamomi on monitored sites in the Grampians, Western Victoria. Australian Journal of Botany 34, 251–279.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lowman MD , Nadkarni NM (1995) ‘Forest canopies.’ (Academic Press: San Diego, CA)

McCredie TA, Dixon KW, Sivasithamparam K (1985) Variability in the resistance of Banksia L.f. species to Phytophthora cinnamomi Rands. Australian Journal of Botany 33, 629–637.
Crossref | GoogleScholarGoogle Scholar | open url image1

McDougall KL, Hobbs RJ, Hardy GEStJ (2002) Vegetation of Phytophthora cinnamomi-infested and adjoining uninfested sites in the northern jarrah (Eucalyptus marginata) forest of Western Australia. Australian Journal of Botany 50, 277–288.
Crossref | GoogleScholarGoogle Scholar | open url image1

McDougall KL, Hobbs RJ, Hardy GEStJ (2005) Distribution of understorey species in forest affected by Phytophthora cinnamomi in south-western Western Australia. Australian Journal of Botany 53, 813–819.
Crossref | GoogleScholarGoogle Scholar | open url image1

Monks L, Coates D (2002) The translocation of two critically endangered Acacia species. Conservation Science Western Australia 4, 54–61. open url image1

Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Newell GR (1998) Characterization of vegetation in an Australian open forest community affected by cinnamon fungus (Phytophthora cinnamomi): implications for faunal habitat quality. Plant Ecology 137, 55–70.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pignatti-Wikus E, Riedl-Dorn C, Mabberly DJ (2000) Ferdinand Bauer’s field drawings of endemic Western Australian plants made at King George Sound and Lucky Bay, December 1801–January 1802. Part II. Rendiconti Lincei. Scienze Fisiche e Naturali 11, 201–244. open url image1

Pilbeam RA, Colquhoun IJ, Shearer B, Hardy GEStJ (2000) Phosphite concentration: its effect on phytotoxicity symptoms and colonisation by Phytophthora cinnamomi in three understorey species of Eucalyptus marginata forest. Australasian Plant Pathology 29, 86–95.
Crossref | GoogleScholarGoogle Scholar | open url image1

Podger FD (1989) Comparative pathogenicity of fourteen Australian isolates of Phytophthora cinnamomi determined on transplants of Tasmanian temperate heathland. Australian Journal of Botany 37, 491–500. open url image1

Podger FD, Doepel RF, Zentmyer GA (1965) Association of Phytophthora cinnamomi with a disease of Eucalyptus marginata forest in Western Australia. Plant Disease Reporter 49, 943–947. open url image1

Reiter N, Weste G, Guest D (2004) The risk of extinction resulting from disease caused by Phytophthora cinnamomi to endangered, vulnerable or rare plant species endemic to the Grampians, western Victoria. Australian Journal of Botany 52, 425–433.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schutte GC, Bezuidenhout JJ, Kotze JM (1991) Timing of application of phosphonate fungicides using different application methods as determined by means of gas–liquid–chromatography for Phytophthora root rot control of citrus. Phytophylactica 23, 69–71. open url image1

Shearer BL (1994) The major plant pathogens occurring in native ecosystems of south-western Australia. Journal of the Royal Society of Western Australia 77, 113–122. open url image1

Shearer BL (2003) The contribution of research in the Forest Department and the Department of Conservation and Land Management to the fight against Phytophthora species in native vegetation of south-western Australia over the last two decades. In ‘Phytophthora in forests and natural ecosystems’. 2nd international IUFRO working party 7.02.09 meeting, Albany, WA. (Eds JA McComb, GEStJ Hardy, IC Tommerup) pp. 235–242. (Murdoch University Print: Perth)

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Shearer BL , Fairman RG (1997 a) Foliar application of phosphite delays and reduces the rate of mortality of three Banksia species in communities infested with Phytophthora cinnamomi. In ‘Proceedings of the 11th biennial conference of the Australasian Plant Pathology Society’. p. 180. (Australasian Plant Pathology Society: Perth)

Shearer BL , Fairman RG (1997 b) Phosphite inhibits lesion development of Phytophthora cinnamomi for at least four years following trunk injection of Banksia species and Eucalyptus marginata. In ‘Proceedings of the 11th biennial conference of the Australasian Plant Pathology Society’. p. 181. (Australasian Plant Pathology Society: Perth)

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. open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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 , Wilcoxson RD (1980) Sporulation of Septoria species on wheat and barley in Minnesota. Agricultural Experimental Station Technical Bulletin 323. University of Minnesota, St Paul, MN.

Shearer BL, Michaelsen BJ, Somerford PJ (1988) Effects of isolate and time of inoculation on invasion of secondary phloem of Eucalyptus spp. and Banksia grandis by Phytophthora spp. Plant Disease 72, 121–126.
Crossref |
open url image1

Shearer BL, Crane CE, Cochrane A (2004a) 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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Shearer BL, Crane CE, Fairman RG (2004b) Phosphite reduces disease extension of a Phytophthora cinnamomi front in Banksia woodland, even after fire. Australasian Plant Pathology 33, 249–254.
Crossref | GoogleScholarGoogle Scholar | open url image1

Shearer B, Crane C, Cochrane A (2005) A thief of time: Phytophthora cinnamomi and threatened flora. Australian Plant Conservation 13(4), 14–15. open url image1

Shearer BL, Fairman RG, Grant MJ (2006) Effective concentration of phosphite in controlling Phytophthora cinnamomi following stem injection of Banksia species and Eucalyptus marginata. Forest Pathology 36, 119–135.
Crossref | GoogleScholarGoogle Scholar | open url image1

Simberloff D, Parker IM, Windle PN (2005) Introduced species policy, management, and future research needs. Frontiers in Ecology and Environment 3, 12–20. open url image1

Smith BJ (1994) Effects of phosphonic acid and sodium silicate on lesion development of Phytophthora cinnamomi and histological responses in host species endemic to Western Australia. BSc(Honours) Thesis. University of Western Australia, Perth.

Stukely MJC, Crane CE (1994) Genetically based resistance of Eucalyptus marginata to Phytophthora cinnamomi. Phytopathology 84, 650–656.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tippett JT, Hill TC, Shearer BL (1985) Resistance of Eucalyptus species to invasion by Phytophthora cinnamomi. Australian Journal of Botany 33, 409–418.
Crossref |
open url image1

Tippett JT, McGrath JF, Hill TC (1989) Site and seasonal effects on susceptibility of Eucalyptus marginata to Phytophthora cinnamomi. Australian Journal of Botany 37, 481–490.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tynan KM, Wilkinson CJ, Holmes JM, Dell B, Colquhoun IJ, McComb JA, Hardy GEStJ (2001) The long-term ability of phosphite to control Phytophthora innamomi in two native plant communities of Western Australia. Australian Journal of Botany 49, 761–770.
Crossref | GoogleScholarGoogle Scholar | open url image1

Vitousek PM, D’Antonio CM, Loope LL, Rejmanek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. New Zealand Journal of Ecology 21, 1–16. open url image1

Weste G (1986) Vegetation changes associated with invasion by Phytophthora cinnamomi of defined plots in the Brisbane Ranges, Victoria, 1975–1985. Australian Journal of Botany 34, 633–648.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Weste G, Kennedy J (1997) Regeneration of susceptible native species following decline of Phytophthora cinnamomi over a period of 20 years on defined plots in the Grampians, Western Victoria. Australian Journal of Botany 45, 167–190.
Crossref | GoogleScholarGoogle Scholar | open url image1

Weste GM, Taylor P (1971) The invasion of native forest by Phytophthora cinnamomi I. Brisbane Ranges, Victoria. Australian Journal of Botany 19, 281–294.
Crossref | GoogleScholarGoogle Scholar | open url image1

Weste G, Cooke D, Taylor P (1973) The invasion of native forest by Phytophthora cinnamomi II. Post-infection vegetation patterns, regeneration, decline in inoculum, and attempted control. Australian Journal of Botany 21, 13–29.
Crossref | GoogleScholarGoogle Scholar | open url image1

Western Australian Herbarium (1998) ‘FloraBase—The Western Australia flora.’ (Department of Environment and Conservation) http://florabase.calm.wa.gov.au/

Wilkinson CJ, Holmes JM, Tynan KM, Colquhoun IJ, McComb JA, Hardy GEStJ, Dell B (2001) Ability of phosphite applied in a glasshouse trial to control Phytophthora cinnamomi in five plant species native to Western Australia. Australasian Plant Pathology 30, 343–351.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wills RT (1993) The ecological impact of Phytophthora cinnamomi in the Stirling Range National Park, Western Australia. Australian Journal of Ecology 18, 145–159.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zadoks JC , Schein RD (1979) ‘Epidemiology and plant disease management.’ (Oxford University Press: New York)