Long-term surveillance of Phytophthora cinnamomi reveals no evidence of increased detections and new insights for monitoring and management

T. J. Mason; K. L. McDougall; P. Craven; C. C. Simpson; G. C. Popovic; D. A. Keith

doi:10.1071/BT24037

RESEARCH ARTICLE (Open Access)

Next Contents Vol 73(1)

Long-term surveillance of Phytophthora cinnamomi reveals no evidence of increased detections and new insights for monitoring and management

T. J. Mason

^A ^B ^* , K. L. McDougall ^B ^C , P. Craven ^D , C. C. Simpson ^B , G. C. Popovic ^E and D. A. Keith ^A

+ Author Affiliations

- Author Affiliations

^A Centre for Ecosystem Science, UNSW Sydney, Sydney, NSW, Australia.

^B Department of Climate Change, Energy, the Environment and Water, Sydney, NSW, Australia.

^C Department of Environment and Genetics, La Trobe University, Bundoora, Vic, Australia.

^D P.O. Box 1093, Tomerong, NSW, Australia.

^E Stats Central, Mark Wainwright Analytical Centre, UNSW Sydney, Sydney, NSW, Australia.

^* Correspondence to: t.mason@unsw.edu.au

Handling Editor: Ben Gooden

Australian Journal of Botany 73, BT24037 https://doi.org/10.1071/BT24037

Submitted: 5 June 2024 Accepted: 27 November 2024 Published: 3 January 2025

Abstract

Context

Phytophthora cinnamomi Rands is an introduced soil-borne pathogen that causes population decline in susceptible species and changes native vegetation compositions. Land managers require information about changing disease incidence, predisposing site factors and potential efficiencies in field identification of the disease. Previous sampling for P. cinnamomi in southern Sydney conservation reserves has provided a framework to monitor pathogen incidence.

Aims

We specifically asked: (1) Is the incidence of P. cinnamomi disease intensifying, decreasing or stable? (2) Is visual assessment of disease symptoms at the community or sentinel species level a good predictor of positive P. cinnamomi laboratory assays? (3) Is the incidence of P. cinnamomi related to access, vegetation type, human visitation or landscape position?

Methods

We assembled data from historic surveys in Dharawal Reserves in 2008 (n = 26) and 2014 (n = 110), and undertook additional surveys in 2022 (n = 110). We supplemented detections in 2008 with 2006–2008 records from other southern Sydney conservation reserves (n = 147). We used laboratory detection results, field observations of plant symptoms and environmental data to assess trends.

Key results

We did not find evidence of increased pathogen incidence over time; however, detection was spatially and temporally variable among sites. Proximity to waterways appeared to increase the likelihood of P. cinnamomi presence. We found differences between visual field assessment of disease expression and laboratory assay of pathogen detection. We observed marginal improvement in detection agreement when we subsetted the data to sites that explicitly identified Xanthorrhoea sp. as potential host species. A sample size analysis indicated that considerable increase in sampling effort would be required to detect consequential changes in the long-term P. cinnamomi status.

Conclusions

Landscape-scale monitoring of P. cinnamomi incidence requires greater sampling intensity and duration to support reliable inferences about trends. Locally focused management and monitoring efforts that consider susceptible sentinel species dynamics may inform the protection of specific assets at risk from infection by P. cinnamomi.

Keywords: diffuse invasion front, Hawkesbury sandstone vegetation, long-term monitoring, pathogen detection, sample size analysis, sentinel species, temporal study, water mould.

References

Anon (2018) Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi. Department of the Environment and Energy, Canberra.

Anon (2019) Annual visits to NPWS Managed Parks in New South Wales. Roy Morgan Research, Melbourne. Available at https://www.environment.nsw.gov.au/-/media/OEH/Corporate-Site/Documents/Research/Our-science-and-research/annual-visits-npws-managed-parks-nsw-state-final-report-august-2019.pdf

Anon (2022a) State of the forests Tasmania 2022 data report. Forest Practices Authority, Hobart, Tasmania. Available at https://fpa.tas.gov.au/__data/assets/pdf_file/0007/521548/Tas_SOF_data_report_2022_final_28_March_2023.pdf

Anon (2022b) Phytophthora (dieback) control environmental instruction. South Australia Department for Infrastructure and Transport, SADfIa Transport. Available at https://www.dit.sa.gov.au/documents

Barrett S, Rathbone D (2018) Long-term phosphite application maintains species assemblages, richness and structure of plant communities invaded by Phytophthora cinnamomi. Austral Ecology 43, 360-374.
| Crossref | Google Scholar |

Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Mächler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal 9(2), 378-400.
| Crossref | Google Scholar |

Brown J, York A (2017) Fire, food and sexual deception in the neighbourhood of some Australian orchids. Austral Ecology 42, 468-478.
| Crossref | Google Scholar |

Burgess TI, Scott JK, McDougall KL, Stukely MJC, Crane C, Dunstan WA, Brigg F, Andjic V, White D, Rudman T, Arentz F, Ota N, Hardy GESJ (2017) Current and projected global distribution of Phytophthora cinnamomi, one of the world’s worst plant pathogens. Global Change Biology 23, 1661-1674.
| Crossref | Google Scholar | PubMed |

Cahill DM, Rookes JE, Wilson BA, Gibson L, McDougall KL (2008) Phytophthora cinnamomi and Australia’s biodiversity: impacts, predictions and progress towards control. Australian Journal of Botany 56, 279-310.
| Crossref | Google Scholar |

Cardillo E, Acedo A, Abad E (2018) Topographic effects on dispersal patterns of Phytophthora cinnamomi at a stand scale in a Spanish heathland. PLoS ONE 13(3), e0195060.
| Crossref | Google Scholar | PubMed |

Carter R (2004) Arresting Phytophthora dieback: the biological bulldozer. WWF and Dieback Consultative Council. Available at https://forestphytophthoras.org/sites/default/files/educational_materials/dieback_report.pdf

Craven P, McDougall K (2015) Occurrence of the plant pathogen Phytophthora cinnamomi at Dharawal National Park. Office of Environment and Heritage, Nowra. Available at https://www.ipcn.nsw.gov.au/resources/pac/media/files/pac/project-submissions/2020/10/dendrobium-extension-project-ssd-8194/20201215t170337/occurrence-of-phytophthora-cinnamomi-at-dharawal-np6271.pdf

Davison EM, Tay FCS (2005) How many soil samples are needed to show that Phytophthora is absent from sites in the south-west of Western Australia? Australasian Plant Pathology 34, 293-297.
| Crossref | Google Scholar |

Dell B, Hardy G, O’Gara E, Shearer B (2007) The impact of Phytophthora cinnamomi on ecosystem function and health of Mediterranean forests, woodlands and heathlands in Western Australia. In ‘Proceedings of the MEDECOS XI Conference’. pp. 69–70. (MEDECOS XI: Perth)

Drenth A, Sendall B (2001) ‘Practical guide to detection and identification of Phytophthora.’ (CRC for Tropical Plant Protection: Brisbane)

Dundas SJ, Fleming PA, Hardy GESJ (2013) Flower visitation by honey possums (Tarsipes rostratus) in a coastal banksia heathland infested with the plant pathogen Phytophthora cinnamomi. Australian Mammalogy 35, 166-174.
| Crossref | Google Scholar |

Fleming PJS, Ballard G, Reid NCH, Tracey JP (2017) Invasive species and their impacts on agri-ecosystems: issues and solutions for restoring ecosystem processes. The Rangeland Journal 39, 523-535.
| Crossref | Google Scholar |

Fraser LR (1956) Phytophthora cinnamomi attacking native plants. Australian Plant Disease Recorder 8, 12.
| Google Scholar |

Garkaklis MJ, Calver MC, Wilson BA, Hardy GES (2004) Habitat alteration caused by an introduced plant disease, Phytophthora cinnamomi: a potential threat to the conservation of Australian forest fauna. In ‘Conservation of Australia’s forest fauna’. 2nd edn. (Ed. D Lunney) pp. 899–913. (Royal Zoological Society of New South Wales: Mosman)

Hardham AR (2005) Phytophthora cinnamomi. Molecular Plant Pathology 6(6), 589-604.
| Crossref | Google Scholar | PubMed |

Hill TCJ, Tippett JT, Shearer BL (1994) Invasion of Bassendean dune Banksia woodland by Phytophthora cinnamomi. Australian Journal of Botany 42, 725-738.
| Crossref | Google Scholar |

Hodges JS, Reich BJ (2010) Adding spatially-correlated errors can mess up the fixed effect you love. The American Statistician 64(4), 325-334.
| Crossref | Google Scholar |

Hüberli D, Hardy GESJ, White D, Williams N, Burgess TI (2013) Fishing for Phytophthora from Western Australia’s waterways: a distribution and diversity survey. Australasian Plant Pathology 42, 251-260.
| Crossref | Google Scholar |

Jurskis V (2005) Eucalypt decline in Australia, and a general concept of tree decline and dieback. Forest Ecology and Management 215, 1-20.
| Crossref | Google Scholar |

Kearney SG, Carwardine J, Reside AE, Fisher DO, Maron M, Doherty TS, Legge S, Silcock J, Woinarski JCZ, Garnett ST, Wintle BA, Watson JEM (2019) The threats to Australia’s imperilled species and implications for a national conservation response. Pacific Conservation Biology 25, 231-244.
| Crossref | Google Scholar |

Keighery G, Gosper CR, Barrett S, Coates D, Makinson RO (2023) The compounding impacts of disease and weeds after the 2019-20 wildfires on Australian vascular plants and communities. In ‘Australia’s megafires: Biodiversity impacts and lessons from 2019–2020’. (Eds L Rumpff, SM Legge, S van Leeuwen, BA Wintle, JCZ Woinarski) p. 512. (CSIRO Publishing: Melbourne)

Keith DA, McDougall KL, Simpson CC, Walsh JL (2012) Spatial analysis of risks posed by root rot pathogen Phytophthora cinnamomi: implications for disease management. Proceedings of the Linnean Society of NSW 134, B147-B179.
| Google Scholar |

Lambeck RJ (1997) Focal species: a multi-species umbrella for nature conservation. Conservation Biology 11, 849-856.
| Crossref | Google Scholar |

Lambers H, Ahmedi I, Berkowitz O, Dunne C, Finnegan PM, Hardy GESJ, Jost R, Laliberté E, Pearse SJ, Teste FP (2013) Phosphorus nutrition of phosphorus-sensitive Australian native plants: threats to plant communities in a global biodiversity hotspot. Conservation Physiology 1, cot010.
| Crossref | Google Scholar | PubMed |

Laurence MH, Mertin AA, Pang C, Wildman O, Daly AM, Summerell BA (2023) First report of Phytophthora plurivora in Australia. Australasian Plant Disease Notes 18, 33.
| Crossref | Google Scholar |

Lenth RV (2022) emmeans: estimated marginal means, aka least-squares means, R package version 1.7.2. Available at https://github.com/rvlenth/emmeans

Lindenmayer DB, Likens GE (2010) The science and application of ecological monitoring. Biological Conservation 143, 1317-1328.
| Crossref | Google Scholar |

Lindenmayer DB, Gibbons P, Bourke M, Burgman M, Dickman CR, Ferrier S, Fitzsimons J, Freudenberger D, Garnett ST, Groves C, Hobbs RJ, Kingsford RT, Krebs C, Legge S, Lowe AJ, McLean R, Montambault J, Possingham H, Radford J, Robinson D, Smallbone L, Thomas D, Varcoe T, Vardon M, Wardle G, Woinarski JCZ, Zerger A (2012) Improving biodiversity monitoring. Austral Ecology 37, 285-294.
| Crossref | Google Scholar |

Magurran AE, Baillie SR, Buckland ST, Dick JMP, Elston DA, Scott EM, Smith RI, Somerfield PJ, Watt AD (2010) Long-term datasets in biodiversity research and monitoring: assessing change in ecological communities through time. Trends in Ecology & Evolution 25, 574-582.
| Crossref | Google Scholar | PubMed |

McDougall KL, Liew ECY (2024) Dispersal of Phytophthora species by off-road vehicles in New South Wales. Australasian Plant Pathology 53, 63-65.
| Crossref | Google Scholar |

McDougall KL, Summerell BA (2003) The impact of Phytophthora cinnamomi on the flora and vegetation of New South Wales - a re-appraisal. In ‘Phytophthora in forests and natural ecosystems, 2nd International IUFRO Working Party 7.02.09 Meeting’, 30 September−5 October 2001, Albany, WA’. pp. 49–56. (Murdoch University: Albany, WA)

McDougall KL, Barrett S, Velzeboer R, Cahill DM, Rudman T (2024) Evaluating the risk to Australia’s flora from Phytophthora cinnamomi. Australian Journal of Botany 72, BT23086.
| Crossref | Google Scholar |

Metz MR, Varner JM, Frangioso KM, Meentemeyer RK, Rizzo DM (2013) Unexpected redwood mortality from synergies between wildfire and an emerging infectious disease. Ecology 94(10), 2152-2159.
| Crossref | Google Scholar | PubMed |

Moore N, Barrett S, Howard K, Craig MD, Bowen B, Shearer B, Hardy G (2014) Time since fire and average fire interval are the best predictors of Phytophthora cinnamomi activity in heathlands of south-western Australia. Australian Journal of Botany 62, 587-593.
| Crossref | Google Scholar |

Murphy B, Vaze J, Teng J, Tuteja NK, Gallant J, Summerell G, Young J, Wild J (2005) Modelling landscapes using terrain analysis to delineate landforms and predict soil depths - examples from catchments in NSW. In ‘Proceedings of the MODSIM International Congress on modelling and simulation’. pp. 1423–1429. (Modelling and Simulation Society of Australia and New Zealand: Canberra)

Nakova M (2010) Monitoring of Phytophthora species on fruit trees in Bulgaria. European Journal of Plant Pathology 128, 517-525.
| Crossref | Google Scholar |

Newby Z-J (2014) Quantification of the risk of Phytophthora dieback in the Greater Blue Mountains World Heritage Area. PhD thesis, University of Sydney, Sydney.

Newby Z, Murphy RJ, Guest DI, Ramp D, Liew ECY (2019) Detecting symptoms of Phytophthora cinnamomi infection in Australian native vegetation using reflectance spectrometry: complex effects of water stress and species susceptibility. Australasian Plant Pathology 48, 409-424.
| Crossref | Google Scholar |

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

Newhook FJ, Podger FD (1972) The role of Phytophthora cinnamomi in Australian and New Zealand forests. Annual Review of Phytopathology 10, 299-326.
| Crossref | Google Scholar |

Noss RF (1990) Indicators for monitoring biodiversity: a hierarchical approach. Conservation Biology 4(4), 355-364.
| Crossref | Google Scholar |

Oberpriller J, de Souza Leite M, Pichler M (2022) Fixed or random? On the reliability of mixed-effects models for a small number of levels in grouping variables. Ecology and Evolution 12(7), e9062.
| Crossref | Google Scholar | PubMed |

O’Brien PA, Williams N, Hardy GESJ (2009) Detecting Phytophthora. Critical Reviews in Microbiology 35(3), 169-181.
| Crossref | Google Scholar | PubMed |

O’Gara E, Howard K, Wilson B, Hardy GES (2005) Management of Phytophthora cinnamomi for biodiversity conservation in Australia: Part 1 A review of current management. Centre for Phytophthora Science and Management, Murdoch University, Western Australia.

Petit S, Dickson CR (2005) Grass-tree (Xanthorrhoea semiplana, Liliaceae) facilitation of the endangered pink-lipped spider orchid (Caladenia syn. Arachnorchis behrii, Orchidaceae) varies in South Australia. Australian Journal of Botany 53, 455-464.
| Crossref | Google Scholar |

Podger FD (1972) Phytophthora cinnamomi, a cause of lethal disease in indigenous plant communities in Western Australia. Phytopathology 62, 972-981.
| Crossref | Google Scholar |

Pratt BH, Heather WA (1972) Method for rapid differentiation of Phytophthora cinnamomi from other Phytophthora species isolated from soil by lupin baiting. Transactions of the British Mycological Society 59(1), 87-96.
| Crossref | Google Scholar |

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.
| Crossref | Google Scholar |

Pyšek P, Hulme PE (2005) Spatio-temporal dynamics of plant invasions: linking pattern to process. Écoscience 12(3), 302-315.
| Crossref | Google Scholar |

R Core Team (2021) ‘R: a language and environment for statistical computing, 4.1.1.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at https://www.R-project.org/

Regan HM, Keith DA, Regan TJ, Tozer MG, Tootell N (2011) Fire management to combat disease: turning interactions between threats into conservation management. Oecologia 167, 873-882.
| Crossref | Google Scholar | PubMed |

Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez J-C, Müller M (2011) pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics 12, 77.
| Crossref | Google Scholar | PubMed |

Samuel G (2020) Independent review of the EPBC Act - Final Report. Department of Agriculture, Water and the Environment, Canberra. Available at https://epbcactreview.environment.gov.au

Schena L, Duncan JM, Cooke DEL (2008) Development and application of a PCR-based ‘molecular tool box’ for the identification of Phytophthora species damaging forests and natural ecosystems. Plant Pathology 57, 64-75.
| Crossref | Google Scholar |

Sena K, Dreaden TJ, Crocker E, Barton C (2018a) Detection of Phytophthora cinnamomi in forest soils by PCR on DNA extracted from leaf disc baits. Plant Health Progress 19, 193-200.
| Crossref | Google Scholar |

Sena K, Crocker E, Vincelli P, Barton C (2018b) Phytophthora cinnamomi as a driver of forest change: implications for conservation and management. Forest Ecology and Management 409, 799-807.
| Crossref | Google Scholar |

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 | Google Scholar |

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 | Google Scholar |

Shearer BL, Crane CE, Cochrane JA, Dunne CP (2013) Variation in susceptibility of threatened flora to Phytophthora cinnamomi. Australasian Plant Pathology 42, 491-502.
| Crossref | Google Scholar |

Smith B, Smith IW, Jones RH, Cunnington J (2009) An evaluation of stream monitoring techniques for surveys for Phytophthora species in Victoria, Australia. In ‘Phytophthoras in forests and natural ecosystems. Fourth IUFRO working party’. p. 325. (US Department of Agriculture: Monterey, California)

Suddaby T (2008) Survey of the distribution of Phytophthora cinnamomi in bushland of the Sydney Metropolitan Catchment Management Authority area. CSMaNDoEaC Change, Sydney.

Suddaby T, Liew E (2008) Best practice management guidelines for Phytophthora cinnamomi within the Sydney Metropolitan Catchment Management Authority area. Botanic Gardens Trust, BG Trust, Sydney. Available at https://catalogue.nla.gov.au/Record/4555713

Summerell BA, Liew E (2020) Phytophthora root rot: its impact in botanic gardens and on threatened species conservation. Sibbaldia: The International Journal of Botanic Garden Horticulture 18, 89-104.
| Crossref | Google Scholar |

Thompson SE, Levin S, Rodriguez-Iturbe I (2014) Rainfall and temperatures changes have confounding impacts on Phytophthora cinnamomi occurrence risk in the southwestern USA under climate change scenarios. Global Change Biology 20, 1299-1312.
| Crossref | Google Scholar | PubMed |

Tozer MG, Turner K, Keith DA, Tindall D, Pennay C, Simpson C, MacKenzie B, Beukers P, Cox S (2010) Native vegetation of southeast NSW: a revised classification and map for the coast and eastern tablelands. Cunninghamia 11(3), 359-406.
| Google Scholar |

von Broembsen S (1984) Distribution of Phytophthora cinnamomi in rivers of the South-Western Cape Province. Phytophylactica 16, 227-229.
| Google Scholar |

Walsh JL, Keith DA, McDougall KL, Summerell BA, Whelan RJ (2006) Phytophthora Root Rot: assessing the potential threat to Australia’s oldest national park. Ecological Management & Restoration 7(1), 55-60.
| Crossref | Google Scholar |

Wan JSH, McDougall KL, Liew ECY (2019) The susceptibility of rare and threatened NSW species to the root-rot pathogen Phytophthora cinnamomi: 1. Initial testing and identification of key research questions. Australian Journal of Botany 67, 510-516.
| Crossref | Google Scholar |

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 | Google Scholar |

Weste G, Marks GC (1987) The biology of Phytophthora cinnamomi in Australasian forests. Annual Review of Phytopathology 25, 207-229.
| Crossref | Google Scholar |

Weste G, Brown K, Kennedy J, Walshe T (2002) Phytophthora cinnamomi infestation - a 24-year study of vegetation change in forests and woodlands of the Grampians, Western Victoria. Australian Journal of Botany 50, 247-274.
| Crossref | Google Scholar |

Wilson BA, Aberton J, Cahill DM (2000) Relationships between site factors and distribution of Phytophthora cinnamomi in the Eastern Otway Ranges, Victoria. Australian Journal of Botany 48, 247-260.
| Crossref | Google Scholar |

Wilson BA, Annett K, Laidlaw WS, Cahill DM, Garkaklis MJ, Zhuang-Griffin L (2020) Long term impacts of Phytophthora cinnamomi infestation on heathy woodland in the Great Otway National Park in south-eastern Australia. Australian Journal of Botany 68, 542-556.
| Crossref | Google Scholar |

Wilson BA, Casey SP, Garkaklis MJ, Learmonth C, Wevill T (2024) Impact of Phytophthora dieback on a key heathland species Xanthorrhoea australis (Asphodelaceae) (austral grasstree) and floristic composition in the eastern Otways, Victoria. Australian Journal of Botany 72, BT23076.
| Crossref | Google Scholar |