Background: Threat abatement plan for disease in natural ecosystems caused by cinnamomi

January 2014 Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi © Copyright Commonwealth of Australia, 2014 ISBN: 978-1-921733-94-9

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Photo credits Front cover: Mondurup Peak, Stirling Range, 2010 (Department of Parks and Wildlife, Western Australia) Back cover: Wildflowers on Mondurup Peak, Stirling Range, 1993 (Rob Olver)

ii / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi Contents 1. Introduction 1

2. Background 2 2.1 The scope of the problem and history of the pathogen in Australia 2 2.2 The pathogen 3 2.2.1 and life cycle 3 2.2.2 Pathogen survival 5 2.2.3 Geographic and climatic occurrence 5 2.2.4 Potential impacts of climate change 8 2.2.5 Transmission and spread 9 2.2.6 Rates of spread 9 2.3 The disease 10 2.3.1 Effects on susceptible plant species 10 2.3.2 Effects on ecological communities 11 2.3.3 Impacts on animals 12 2.3.4 Resistance to infection 13 3. Dealing with the problem 14 3.1 Identification of the disease 14 3.1.1 Detection 14 3.1.2 Diagnosis 14 3.1.3 Mapping 15 3.2 Minimising the spread of Phytophthora cinnamomi 16 3.2.1 Access prohibition or restriction 16 3.2.2 Hygiene 16 3.2.3 Potential further introductions through revegetation 17 3.2.4 Eradication 18 3.2.5 Monitoring and surveillance 18 3.3 Treatment options to mitigate the impact of Phytophthora cinnamomi 18 3.3.1 Phosphite 18 3.3.2 Ex situ conservation 20 3.3.3 In situ conservation 21 3.3.4 Breeding for resistance 21 3.3.5 Other methods of control 21 3.4 Wide scale detection, diagnosis and demarcation protocols 22 3.5 Risk assessment and priority setting 22

iii References 24

Appendix A 29 Data contributions for figure 2 29 Appendix B 30 Suggested reading 30 Further reading 30 Information on other Phytophthora species 33 Appendix C 34 State documents relevant to Phytophthora cinnamomi 34 Appendix D 36 Site variables that influence whether eradication or containment of Phytophthora cinnamomi is possible 36

iv / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi 1. Introduction Australia’s native plants and ecological communities are threatened by the soil-borne plant pathogen, Phytophthora cinnamomi, for which it is estimated there are over 2000 potential host species (Shearer et al., 2004).

P. cinnamomi is present in all states and territories of This background document complements the Australia and causes disease in an extremely diverse statutory Threat abatement plan for disease in natural range of native, ornamental, forestry and horticultural ecosystems caused by Phytophthora cinnamomi (TAP) plants. Described as a ‘biological bulldozer’, (Department of the Environment, 2014). The TAP P. cinnamomi is destroying bushlands, heathlands, outlines the actions proposed to abate the threat and woodlands and forests, which are the habitat for rare addresses statutory requirements. This document and endangered flora and fauna species. ‘Dieback provides supporting information on matters such as caused by the root-rot fungus Phytophthora the biology of the pathogen, its population dynamics, cinnamomi’ is listed as a key threatening process under spread, diagnosis and impacts on biodiversity and the Environment Protection and Biodiversity management measures. Conservation Act 1999 (EPBC Act).

1 2. Background

2.1 The scope of the problem Other evidence for P. cinnamomi being non-endemic is that most occurrences follow human occupation, and history of the land use and activities. pathogen in Australia P. cinnamomi can parasitise a wide range of life stages P. cinnamomi was first described on the island of across the taxonomic spectrum of Australian flora. Sumatra, Indonesia, in 1922, as the cause of stripe It reacts with its hosts in a number of distinct ways, canker on cinnamon trees (Rands, 1922). The likely ranging from symptomless infection restricted to root region of origin of the pathogen is Papua New Guinea tissue (for example, in some grasses) to complete (Hardham, 2005) and the known introduced range of invasion of root and stem tissue. P. cinnamomi now includes Europe, North America, The consequences of infection of a susceptible South Africa and the Australasia-Pacific region. ecological community will usually be the following: P. cinnamomi is thought to have entered Australia with • extinction of populations of some flora species early settlers from Europe. Since the mid 1960s this exotic pathogen has been recognised as a cause of • a modification of the structure and composition of serious disease in native ecosystems of Australia. In the ecological communities 1960s, P. cinnamomi was recognised as the cause of • a massive reduction in primary productivity disease in (jarrah) trees in Western Australia, in native forests in East Gippsland • a reduction in the genetic diversity of a plant and in woodlands in the Brisbane Ranges in Victoria species and in the Mount Lofty Ranges of South Australia. • habitat loss and degradation for dependent flora and fauna. Although many root pathogens are known to cause disease in Australian flora species, P. cinnamomi has After the pathogen’s effects on an ecological had the greatest effect and poses the greatest threat. At community have taken their course, the smaller least 32 species of Phytophthora occur in various parts number of resistant species that remain, with time, of Australia. Its patterns of disease and continuing recolonise areas affected by the pathogen. These areas invasion in much of southern Australia are are generally less productive, have more open characteristic of a pathogen newly introduced to an overstorey (altering hydrological and physicochemical environment with susceptible flora. The species can aspects of the soil) and provide a modified habitat for reproduce sexually; however, for this to occur, two dependent fauna and flora. mating strains (A1 and A2) of the pathogen need to be present. The major evidence for the pathogen being A threat of an epidemic exists where dominant species non-endemic to Australia is: of particular plant communities are inherently susceptible to disease caused by P. cinnamomi and 1. The A2 strain of P. cinnamomi predominates in the those communities are in areas where environmental Australian environment. If Australia was the centre conditions favour the pathogen. Warm, wet soils, of origin, a greater balance between the A1 and A2 especially those with impeded drainage, favour strains would be expected. sporulation and movement of P. cinnamomi, as well as its growth within plant tissue. If an interaction that is 2. The high level of susceptibility of many Australian sufficiently destructive to be considered a threatening native species of plant which suggests that the process is to develop, both these conditions need to be plants did not evolve with the pathogen. present.

2 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi Serious epidemics do not necessarily always follow the When mature, sporangia range in size from 50 to arrival of P. cinnamomi into uninfected plant 70 microns (or 0.05 to 0.07 mm) in length. communities and the pathogen can occur in Under favourable conditions (free water and warm environments where the effects are not immediately temperatures) P. cinnamomi readily produces apparent. In some cases visual symptoms may take sporangia. years to manifest after the initial infection. Up to 30 zoospores, each less than 10 microns in diameter, are produced within each sporangium. Zoospores are short-lived (2 to 3 days) and have two 2.2 The pathogen flagella which enable them to swim for short distances through water (25 to 30 millimetres, with soil porosity P. cinnamomi is a microscopic soil-borne organism a factor in how far they will travel). At the end of the that attacks the roots and collar of susceptible plants. motile phase the flagella are lost and the zoospore Depending upon environmental conditions and plant encysts. While all spores have the capacity to directly susceptibility, it can destroy vegetation communities infect plants, zoospores are thought to be the major and several plant species are at risk of extinction (see infection propagule. tables at Appendix A and B in the TAP). In vegetation communities where most dominant plants are resistant Chlamydospores are round, average 41 microns in to P. cinnamomi, it is characterised by the attrition of diameter and are commonly thin-walled, although minor structural components, making disease thick-walled chlamydospores have been observed. detection difficult. The sexually produced oospores are round and thick-walled, with a diameter in the range 19 to 2.2.1 Taxonomy and life cycle 54 microns and are considered highly resistant to P. cinnamomi is often referred to as a fungus because of degradation. Oospores are hard-coated and can its filamentous growth and ability to cause plant withstand dry conditions in soil and in dead plant disease, however, in taxonomic terms it is more closely tissue for many years. Figure 1 shows the generalised related to algae than to fungi. It is sometimes called a life cycle of P. cinnamomi. water mould. Its taxonomic nomenclature is: Kingdom: Chromista, Phylum: Oomycota, Order: , Family: , Genus: Phytophthora, Species: cinnamomi.

In the vegetative state, P. cinnamomi occurs as mycelia, which consist of branched filaments termed hyphae. Two types of spores are produced asexually by the mycelium: zoospores, that are produced within structures called sporangia and chlamydospores. A third type of spore, termed an oospore, is produced through sexual recombination of A1 and A2 mating strains of the pathogen.

3 Figure 1 Generalised life cycle of Phytophthora cinnamomi (Diagram courtesy of Professor A Hardham, Australian National University, Canberra, ACT, published in Hardham (1999)).

When a zoospore encounters a root, the zoospore-cyst the functions affected, and this is why symptoms of produces a germ-tube which chemically and physically P. cinnamomi infection have similarities, at least breaches the protective surface of the root. Once initially, with those of water-stress. inside the plant the germ-tube develops into mycelium As the A2 mating strain predominates in the and grows between, and into, the plant cells. The Australian environment, it is unlikely that sexual pathogen may exit the infected root at some point, recombination, and thus oospore production, occurs starting new infections. to any large degree in the natural environment. The plant becomes visibly diseased when infection results in the impairment of the plant’s physiological and biochemical functions. Uptake of water is one of

4 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi 2.2.2 Pathogen survival The areas of Australia vulnerable to disease caused There are still significant gaps in our knowledge of the by P. cinnamomi can be separated into five broad exact mechanisms of long-term pathogen survival. climatic zones: Of the asexual spores, chlamydospores are thought to • north Queensland in elevations above 750 metres be the most resistant to degradation and have, with notophyll dominant vegetation and therefore, been implicated in the ability of acid-igneous geology P. cinnamomi to survive for long periods of time under unfavourable conditions. They potentially provide a • northern New South Wales/southern Queensland source for re-infection of seedlings or long distance border region spread via soil movement. • areas of Mediterranean climate (warm to hot, dry summers and mild to cool, wet winters) where Crone et al. (2013) claim that their recent study has annual rainfall exceeds 600 millimetres, in shown, for the first time, the importance of selfed southern Western Australia and South Australia oospores—thick walled chlamydospores and stromata and southern Victoria as far east as Wilsons produced by P. cinnamomi in asymptomatic annual Promontory and herbaceous perennial species—for the long term survival of P. cinnamomi. They also claim it has • areas with moderate temperature variation, but increased our understanding of a biotrophic and/or erratic rainfall regimes—at low elevations of the endophytic lifestyle of P. cinnamomi in these plant coastal plain and foothills between Wilsons species not previously recognised as hosts of the Promontory and south of the Victoria and pathogen. New South Wales border • winter-dominant rainfall areas, in maritime climates of coastal and sub-montane Tasmania. 2.2.3 Geographic and climatic occurrence Recent work by Newby (2013) on vulnerable areas in The magnitude of the impact of P. cinnamomi in a the Greater Blue Mountains World Heritage Area has native vegetation community is determined by a considered the climate and/or landscape suitability for combination of factors including temperature, rainfall P. cinnamomi via species distribution models. It was and soil types. The area of native vegetation affected found that P. cinnamomi was most likely to be found by P. cinnamomi exceeds a million hectares in Western where rainfall was 1300 millimetres per annum Australia, many hundreds of thousands of hectares in and would not be found below 550 millimetres Victoria and Tasmania and tens of thousands of per annum. It was also most likely to occur where hectares in South Australia. minimum temperatures were between 11 to 13°C and not found where the minimum temperature did not In Australia, P. cinnamomi does not usually cause drop below 18°C. P. cinnamomi was best suited to soils severe impacts in undisturbed vegetation at sites with ~6-8 per cent clay, but past ~37 per cent, it was that receive a mean annual rainfall of less than unlikely to occur. Many of the most conducive areas 600 millimetres, and are north of latitude 30° were, but not limited to, high altitudes in the range of (O’Gara et al., 2005b). While rainfall is a key factor 900 to 1000 metres. influencing the distribution of disease caused by P. cinnamomi, there are many other factors that Although rainfall is clearly sufficient for the influence disease expression (i.e. conducive establishment of P. cinnamomi in the wet/dry, true and temperature, geology and soil conditions co-occurring sub-tropical north of Australia, there are scant data to with susceptible plant hosts, including pH, fertility, indicate that P. cinnamomi is a problem in undisturbed moisture and texture). native ecosystems of northern Western Australia or the Northern Territory.

5 P. cinnamomi is known to occur in coastal (Gadek and Worboys, 2003, cited in O’Gara et al., Queensland. Although considered to be restricted to 2005a). the wet coastal forests, many of these areas are Speculation still exists over the role of P. cinnamomi in designated as conservation reserves or state forests and damage to undisturbed montane regions above 800 are managed for recreation and conservation purposes. metres, such as those found in the southern Great Visitor access, and therefore the risk of spread of Dividing Range, the Central Highlands of Tasmania, P. cinnamomi, is also considered a problem that will and the upland and highland rainforests of central and need to be addressed. Additionally, P. cinnamomi is a far north Queensland. serious concern in the Wet Tropics World Heritage region of far northern Queensland, where the P. cinnamomi isolations, records of impact and the syndrome is complex, differs considerably from that in broad climatic envelope of P. cinnamomi susceptibility the temperate south of the continent and appears to in Australia are depicted in Figure 2. be related to prior significant disturbance of sites

Figure 2 P. cinnamomi isolations, records of impact and broad climatic envelope of P. cinnamomi susceptibility in Australia. Based on O’Gara et al. (2005b) and occurrence data supplied to DSEWPaC between 2010 and 2012 (contributors are listed at Appendix A). This figure does not represent the precise distribution of the pathogen in Australia and is for general information only. It is not intended to be used for management purposes.

6 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi Areas of susceptibility and • the temperate rainfall regimes at low elevations of distribution the coastal plain and the foot hills of Wilsons Promontory Some states in Australia have identified broad zones where biodiversity assets are susceptible to the threat • south of the border between Victoria and of P. cinnamomi. The environmental criteria used to New South Wales. identify these zones vary from state to state and are summarised below. The biomes that appear to be least South Australia threatened are the wet–dry tropics and the arid and semi-arid regions of the continent (Environment In South Australia, any site with susceptible vegetation Australia, 2001). growing on neutral to acid soils and an average annual rainfall greater than 400 millimetres is considered vulnerable to the threat of P. cinnamomi (Phytophthora Western Australia Technical Group, 2006). In Western Australia the vulnerable zone was defined The present known distribution in South Australia by the Department of Conservation and Land includes numerous Conservation and National Parks, Management (2003) as: Forest Reserves and many roadside reserves in the • the parts of the South West Land Division and Mount Lofty Ranges, Fleurieu Peninsula and on areas adjoining it to the north-west and south-east Kangaroo Island. P. cinnamomi is also suspected to be that receive an average annual rainfall greater than present on Lower Eyre Peninsula. 400 millimetres • those areas receiving rainfall above 400 millimetres New South Wales and the that do not have a calcareous substrate and in Australian Capital Territory which susceptible native plants occur in Clear criteria for what constitutes an area’s conjunction with the environmental factors vulnerability to the threat of P. cinnamomi in required for P. cinnamomi to establish and persist. New South Wales and the Australian Capital Territory are not available for two major reasons: Tasmania • There is insufficient knowledge of the susceptible The vulnerable zones of Tasmania include areas where species in New South Wales and the Australian there is a coincidence of: Capital Territory. • susceptible native vegetation in open communities • There is variable susceptibility of plant species • non-calcareous soils depending on climatic conditions, i.e. some species only appear susceptible during sustained periods of • elevation below 700 metres unusually high rainfall. • average annual rainfall greater than 600 millimetres. In New South Wales, P. cinnamomi causes large-scale disruption of native ecosystems and is known to occur in a number of National Parks and Nature Reserves. Victoria The full extent of distribution of P. cinnamomi Where susceptible native species or communities of throughout New South Wales is largely unknown due plants occur, the areas in Victoria that are considered to survey limitations. However, recent surveys indicate vulnerable to the threat of P. cinnamomi are: that the pathogen is more widespread than previously thought. • all elevations in those sites of Mediterranean climate from the west of the state across to Wilsons Promontory where average annual rainfall exceeds 600 millimetres

7 Queensland a 10 per cent decrease, depending on the model used The average annual rainfall in the wet tropics of far (CSIRO and Bureau of Meteorology, 2007, 2012). A north Queensland is rarely limiting for the major reduction in rainfall could reduce the impact of establishment of P. cinnamomi. As with New South the pathogen in some areas. In contrast, increased Wales and the Australian Capital Territory, the evaporation rates resulting from higher temperatures pathogen tends to have a cryptic nature and is and more frequent extreme rainfall events could lead frequently isolated from soils beneath symptom-free to greater runoff and pathogen dispersal (Cahill et al., vegetation. However, plant disease attributed to 2008). Furthermore, stress in native plant P. cinnamomi in natural tropical ecosystems of far communities resulting from altered climatic north Queensland is commonly associated with some conditions could interact with the disease caused by prior disturbance (particularly roads) on sites that have P. cinnamomi. the following characteristics: A recent study (CPSM, 2013) used existing datasets • elevation above 750 metres on P. cinnamomi distribution together with strategic soil surveys from regions outside the pathogen’s known • notophyll dominant vegetation distribution range. It used CLIMEX modeling to • acid-igneous geology (Worboys and Gadek, 2004, determine its likely distribution in 2070 based on the cited in O’Gara et al., 2005a). CSIRO-Mk3.0 global climate model. The modeling demonstrates that in the future, areas with previously Although dieback related to P. cinnamomi is reported unfavourable conditions, particularly at altitudes in upland subtropical rainforests of the Eungella above 700 m, may lead to an increase in disease Plateau, west of Mackay, and from the wallum incidence as these regions become warmer over time. heathlands in the south-east of the state, there has In addition, in areas where rainfall is predicted to been no assessment of what criteria may be useful in decrease, disease incidence is likely to decline. This is categorising vulnerable vegetation. the most comprehensive study of P. cinnamomi distribution undertaken to date. The information will Northern Territory be useful to managers and policy makers involved in ensuring the spread and impact of P. cinnamomi is To date there is no confirmed record of P. cinnamomi contained in the future. being associated with disease in undisturbed native vegetation in the Northern Territory. It is generally Seasonal changes can influence the impact and spread accepted that the environmental conditions are not of the pathogen. For example, wetter summers could conducive to the establishment and persistence of be favourable to spread and increase the impact of P. cinnamomi in susceptible native plant communities. P. cinnamomi, and drier winters less so. Any possible reduction in pathogen activity due to reducing winter Cahill et al. (2008) provides a recent and rainfall could be offset by increasing soil temperatures comprehensive review of the regional impact of becoming more conducive to pathogen activity. Lucas P. cinnamomi. (2003) found in glasshouse experiments that simulating a drought over summer increases the resistance of E. marginata (jarrah) to P. cinnamomi. 2.2.4 Potential impacts of climate change Physiological changes in host plants and in the pathogen could also be factors involved in the impact Climate change-induced fluctuations in average of climate change. P. cinnamomi is fully capable of rainfall may change the future distribution of adapting to new environmental conditions and of P. cinnamomi and the manifestation of the disease it developing virulence on new hosts during asexual causes. For example, by 2070 southern regions of growth (Hardham, 2005). Australia are predicted to exhibit differences in average rainfall of between -30 per cent and +5 per cent of For a midrange emission scenario, CSIRO and Bureau current precipitation, with the best estimate of around of Meteorology (2007; 2012) predict a best estimate

8 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi of annual warming over Australia by 2030 of around 25 to 30 millimetres. Mycelia can grow around 1°C. There are likely to be regionally different through roots and spread to adjacent healthy plants responses across Australia. For most locations the where root-to-root contact occurs. Root-to-root mean warming is predicted to be 0.7 to 0.9°C in movement of the pathogen is thought to be one of the coastal areas and 1 to 1.2°C inland. In winter, major ways in which the pathogen spreads up and warming is projected to be a little smaller than in the across slopes from a disease centre. other seasons, as low as 0.5°C in the far south. P. cinnamomi can be carried passively in overland and Warming is usually predicted to be smaller near the subsurface water flow. Animals may also act as vectors coasts than further inland. Annually, predicted results of infested soil and have been implicated in spreading have a similar predicted pattern to the seasons, with P. cinnamomi, particularly where there is digging or the warming being largest in the interior and the soil disturbance behaviours. This movement is greater north-west. on sticky clay soils and wet peats than on drier, For the south- west of Western Australia, where many well-drained soils of low organic content. threatened P. cinnamomi susceptible species occur, Among the numerous P. cinnamomi vectors, human- there is a high level of consistency amongst climate induced transport of soil is the most important. This prediction models for 2050. All suggest a total occurs as a result of road building and maintenance, precipitation decline in south-western Australia from emergency and land management activities, the coast (between three per cent and 22 per cent in commercial activities (such as timber harvesting, Cape Naturaliste and King River) to the inland wheat mineral exploration and the nursery trade) and human belt (between zero per cent and 36 per cent in recreational activities (such as bushwalking and Corrigin) (CSIRO and Bureau of Meteorology, 2007; off-road vehicle activities). In southern Australia, this 2012). For both temperature and precipitation, is especially the case when these activities are projected change can vary significantly at fine spatial undertaken during the southern spring or periods of scales, particularly in coastal and mountainous areas. high summer rainfall, when conditions are most Under these predicted climate scenarios, the frequency conducive to pathogen reproduction and plant of both drought and fire are likely to increase, adding infection. to pressures on listed species (Cochrane et al., 2011). Survival, establishment and further spread are Monitoring the health of high priority susceptible dependent on conditions at the point of delivery, in species and communities over time (for example particular, sufficient moisture for the pathogen and the or grass tree woodland) will provide an presence of living host tissue. The success of indication of the impact of the pathogen on priority establishment for new centres of infection is also native species and communities in a changing climate. dependent on population levels in the soil at the point of pick-up and the quantity transferred. Most of the large centres of infection that exist today in southern 2.2.5 Transmission and spread temperate Australia occurred as a result of human P. cinnamomi can be spread either actively or passively. activity, often as a direct result of introducing infected Active or autonomous dispersal occurs as a result of soil or road-building materials to vulnerable actions on the part of the pathogen—predominantly uninfected areas. by zoospores and mycelial growth. Passive dispersal of the pathogen is dependent upon propagules of the pathogen being passively carried or vectored by an 2.2.6 Rates of spread independent party or object. The time-scale for natural spread depends upon the topography, vegetation and climate. Annual rates of Active spread by zoospores is favoured by coarse- spread at the boundaries of existing infection are textured soils with large pores, and water-filled root highly variable, ranging from a few to hundreds of channels through which zoospores are able to swim for metres down slope in incised water courses or gullies.

9 Surveys in Western Australia have shown the Shrubs generally turn yellow, with dieback occurring P. cinnamomi upslope disease extension on the Darling in warm moist periods during spring and autumn. Plateau (East) was 0.37 metres/year, compared to Infected trees can produce epicormic growth but may 2.15 metres/year for the Blackwood Sedimentary eventually die. Infected plants may appear to recover Plateau where a perched water table provides long when environmental conditions do not favour the periods of favourable conditions conducive to pathogen but dieback often occurs again when the proliferation of the pathogen (Strelein et al., 2006). plant is under environmental stress and the pathogen In the E. marginata (jarrah) forest of Western is active. Australia, upslope and across slope spread seldom The symptoms of disease in Xanthorrhoea (grass tree) exceeds an average of one metre a year (Podger et al. species are caused by a combination of damage to 1996, cited in O’Gara et al., 2005a). tissues of the roots and stem that may lead to a reduction in water and nutrient transport throughout the plant (Aberton et al., 2001). Susceptible 2.3 The disease Xanthorrhoea species such as X. australis, 2.3.1 Effects on susceptible plant X. quadrangulata and X. semiplana often decline rapidly and the plant may collapse (R Velzeboer 2012, species pers. comm.). Disease symptoms may vary between plant species. In the early stages of disease, symptoms generally consist The families from which the pathogen is most of retarded growth and slight drooping of the foliage. frequently isolated are Myrtaceae, Proteaceae, Infected broadleaf species wilt during the heat of the Fabaceae, Epacridaceae and Dilleniaceae. With the day and may recover at night. Roots become exception of the Dilleniaceae, this reflects the discoloured and die. Dark or reddish brown dominance of these families in the woody flora of discoloration may extend up into the wood of the Australia and their importance as structural lower stem. Severely affected plants may wilt components in the affected communities. However, permanently and their leaves turn brown. there is considerable variation in susceptibility within families, genera and species (Cahill et al., 2008). Epidemic disease and the major disruption that occurs to the functioning of plant communities is not the In Western Australia, 300 plant species have been only circumstance that could threaten the extinction listed as susceptible to infection by P. cinnamomi of populations of susceptible plant species. Plant (O’Gara et al., 2005b) although it has been estimated species that exist only as small, localised populations that as many as 2000 plant species of the south-west may be threatened with extinction due to disease are susceptible (Wills, 1993). Shearer et al. (2004) has occurring under less favourable conditions and causing estimated a mean of 40 per cent susceptible and a slow attrition of individuals in those populations. 14 per cent highly susceptible (2284 species and 800 species respectively) for the 5710 described plant A number of flora species which are nationally listed as species in Western Australia’s South-West Botanical being threatened and which may be susceptible to Province. P. cinnamomi are listed in Appendix A of the TAP.

10 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi 1993 2010

Damaged: These before-and-after images of Mondurup Peak, Stirling Range in Western Australia reveal the effects of P. cinnamomi on the landscape. (Left: Rob Olver, right: Department of Parks and Wildlife, Western Australia)

A list of over 1000 native plant species known to be in populations of the listed species. They provide no susceptible to disease by P. cinnamomi in Australia is indication of the extent of invasion or of the severity contained in the National Best Practice Guidelines of the consequences in terms of the health and survival (O’Gara et al., 2005b). The list has been compiled of individual plants, plant populations or species. As a from published material, unpublished records and result they are not very useful for predicting the observations of individual researchers. possible fate of a particular species.

Several problems arise when trying to define the susceptibility of flora species. A highly susceptible species is one that has high mortality in the field but 2.3.2 Effects on ecological this may be influenced by a number of variables at the communities site and other environmental conditions that affect a Infection by P. cinnamomi in susceptible ecological plant’s reaction to infection. For example, the response communities will often result in major disruption and of a species in the wild may depend on static site decline of structure and composition of those conditions (for example substrate and pH) and communities. Further, the vegetation assemblages of temporal conditions (for example rainfall and resistant species that, with time, recolonise areas are disturbances such as fire); species may not be hosts of less species-rich, have more open overstorey and P. cinnamomi at all but may be affected by changes in provide a modified habitat for dependent organisms. vegetative structure caused by the death of surrounding plants or there may be a spatial variation In many high-rainfall areas the biomass of in the response of a host (for example Hibbertia communities can be dramatically impacted. For hypericoides is highly susceptible to infection on the example, in woodlands dominated by species of Swan Coastal Plain of Western Australia but rarely Banksia and Eucalyptus on highly susceptible sites, affected in the adjoining E. marginata (jarrah) forest). basal area (an index of accumulated biomass) reduced It has also been recognised that there can be variability to a fraction of its pre-infection status. in susceptibility within a species, resulting in the same In Victoria, long-term studies have been undertaken species being ascribed different levels of susceptibility in the Brisbane Ranges, Wilsons Promontory National in different areas. Park, Grampians National Park (Weste et al., 2002) At best, records of host species suggest only that and Anglesea (Wilson et al., 1997). Species present in P. cinnamomi is able to infect some part of some plants post-diseased areas are likely to be either resistant to

11 P. cinnamomi, exhibiting little or no disease symptoms, and Laidlaw, 2001). Five rare or threatened species; or tolerant/fluctuating species that exhibit some Pseudomys fumeus (smoky mouse), P. shortridgei (heath disease symptoms as well as showing regrowth and mouse), P. novaehollandiae (New Holland mouse), recovery at times. Longer term studies in the Brisbane Potorous longipes (long-footed potoroo) and Petrogale Ranges and the Grampians have shown penicillata (brush-tailed rock-wallaby), have greater chronosequential changes in the floristic composition than 20 per cent of their distributions in areas (Weste and Ashton, 1994; Weste et al., 2002). susceptible to Phytophthora dieback (Cahill et al., 2008). Crone et al. (2012) showed, for the first time, the importance of annual and herbaceous perennial plants, In New South Wales P. cinnamomi invasion is with and without symptoms, as hosts of P. cinnamomi. considered to be a process threatening the These are important but previously overlooked groups conservation of endemic populations of Isoodon of plants that can allow the pathogen to persist on obesulus (southern brown bandicoot) and P. fumeus sites after susceptible species have disappeared or have (smoky mouse). P. longipes (long-footed potoroo) is substantially reduced in numbers. also considered to be at risk from Phytophthora impact due to the proximity of infections to suitable habitat for this marsupial. 2.3.3 Impacts on animals In South Australia, the endemic and endangered There has been little work investigating the impact of Sminthopsis aitkeni (Kangaroo Island dunnart) is Phytophthora dieback on faunal populations and regarded to be threatened by P. cinnamomi due to the communities. Despite this, there is a concern that the loss of susceptible plants from its habitat (Gates, dramatic impact of P. cinnamomi infections on plant 2011). communities can result in major declines in some animal species due to the loss of shelter and nesting Wilson et al. (1994) found that P. cinnamomi has the sites or food sources. The greatest impact is likely to potential to influence the abundance and composition be to those species that require relatively dense of many faunal communities. These effects are largely species-rich shrublands or have restricted diets. indirect, resulting from changes in plant species’ richness and composition and from alterations to the There are very susceptible plant species in most of the structural compositions of habitat. habitats on the south coast of Western Australia in which the EPBC Act listed Parantechinus apicalis For example, the abundance of Antechinus stuartii (dibbler) has been recorded. The effect of disease- (brown antechinus) was significantly lower at sites induced changes to the habitats of dibblers is infected with P. cinnamomi and a significant unknown but disease caused by P. cinnamomi needs to relationship was found between the capture rate of this be considered as a potential threat (Friend, 2004). species and the volume of vegetation present up to 40 cm above ground level (Newell and Wilson, 1993). Also in Western Australia, the conservation status of A. agilis (agile antechinus), Rattus fuscipes (bush rat), Tarsipes rostratus (honey possum) has been R. lutreolus (swamp rat) and S. leucopus (white footed speculatively connected to Phytophthora dieback dunnart) were captured more frequently in non- (Calver and Dell, 1998). The density and distribution diseased areas as compared to diseased areas. This of the honey possum is governed by the availability of shows that the pathogen may affect the community nectar and pollen for food, predominantly from structure of small mammals, which may lead to a proteaceous plants (Garavanta et al., 2000; Wooller decline in species’ richness as a consequence of the et al., 2000), many species of which are known to be disease proceeding through the habitat (Laidlaw and susceptible to P. cinnamomi. Wilson, 2006). An analysis of mammals that occur in Victoria found that for 22 species, more than 20 per cent of their range occurs in P. cinnamomi-affected areas (Wilson

12 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi Menkhorst and Broome (2006) found that the pathogen once it penetrates the roots and prevent P. cinnamomi has the potential to have a very large it from invading the rest of the root system and plant impact on populations of the EPBC Act listed collar. Other plants, typically monocotyledons, are Endangered P. fumeus (smoky mouse). Many of the able to rapidly produce new roots to replace those plant families and genera characteristic of smoky infected by the pathogen and so are able to withstand mouse habitat are particularly susceptible to the infection. Field observations suggest that in general, pathogen. herbaceous perennials, annuals and geophytes are more resistant to P. cinnamomi than woody perennials.

2.3.4 Resistance to infection Field observations suggest that there is also considerable variation in resistance between species There are few plants that are truly resistant to within the same genus or subgenus. For example, in P. cinnamomi: the pathogen is capable of infecting the the genus Eucalyptus, most species in the subgenus roots of all species that have been tested so far. Many Symphomyrtus (gums, boxes and ironbarks) are species may become infected with P. cinnamomi but relatively resistant to infection by P. cinnamomi, but not all species die as a result of infection. Those most species in the subgenus Monocalyptus (ashes, non-susceptible species that have been examined in stringybarks and peppermints) are susceptible. detail produce a number of responses that will contain the infection to the immediate vicinity of pathogen penetration. Some plants are able to compartmentalise

13 3. Dealing with the problem

The limited management options currently available 3.1 Identification of the focus on the modification of human activities through restricting access to certain sites, and deploying and disease enforcing hygiene procedures to minimise the spread 3.1.1 Detection of P. cinnamomi in the landscape. Currently, the two Current practice in detecting P. cinnamomi in the field major objectives of P. cinnamomi management are: involves the observation of visible symptoms of disease • to prevent the introduction or minimise the spread in vegetation and confirmation of its presence through of P. cinnamomi into uninfected areas sampling and laboratory analysis of soil and diseased plant tissues. • to reduce the impact of P. cinnamomi at infected sites. Aerial photographs (1:4500 nominal scale, but up to 1:25 000) can be used to detect the disease on a broad To manage the problem of P. cinnamomi infection, scale. Given sufficient disease expression, trained a set of tools, skills and protocols has been developed personnel can make decisions about the disease status based on knowledge of P. cinnamomi status and of an area by stereoscopic examination of aerial preferences on a geographical and species basis photographs taken in autumn under shadowless (section 3.1). conditions (full cloud cover). In autumn, infected Active interventions that reduce transmission of plants that have died after making a final effort to P. cinnamomi are projects that involve quarantine or respond to summer drought-breaking rains have access prohibition or restriction, and/or involve a yellow to bright orange leaves and are readily detected hygiene component with disinfection of machinery or via aerial photographs. inanimate objects entering an area free of the pathogen The expected take-up of improvements in detection (section 3.2). techniques using polymerase chain reaction (PCR) The use of the fungistatic agent phosphite directly (O’Brien, 2008) will enable more accurate and applied to the host plant is difficult and expensive to cost-effective detection of P. cinnamomi in infested apply in remote areas, but is useful in localised soil. DNA-based detection offers improved sensitivity populations of high conservation value. However, and higher sample throughput for the detection of there is much still unknown about the effects of the P. cinnamomi than baiting assays. Williams et al. agent on non-target species and animals (section 3.3). (2009), through comparative analysis using PCR- Assessment of the effectiveness of management based methods in parallel with baiting assays, showed regimes requires ongoing monitoring to detect changes a significant increase in the detection of P. cinnamomi in disease status. The integration of these strategies by nested PCR. and the local integration of management techniques in an adaptive management approach will maximise the success of P. cinnamomi management (sections 3.4 3.1.2 Diagnosis and 3.5). There is widespread confusion between the disease and death caused by P. cinnamomi and disease and death resulting from other causes in native vegetation, largely because of the difficulty of field diagnosis. Field diagnosis of disease relies heavily on the specialist interpretation of symptoms produced by indicator species, coupled with knowledge and information

14 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi about potentially confounding environmental factors disease demarcation. PCR-based detection methods such as site and soil characteristics, fire, drought and may reduce the costs of sample analyses. Maps of abiotic or other biotic diseases that may mimic the disease occurrence through interpretation of aerial symptoms of disease caused by P. cinnamomi. This photographs can be developed at a lower cost but they problem is exacerbated by the cryptic nature of do not have the same level of detail as those produced P. cinnamomi. The organism can be seen only by through on-ground survey. In addition, maps derived microscopic examination in laboratories; while it from aerial photography are generally not suitable sometimes produces reliable visible symptoms in a where there is a lack of susceptible species in the dense number of hosts, in many other hosts it is not reliably emergent shrub or forest layer, and the scale of detected. photography often precludes interpretation of disease symptoms under these conditions. Cahill et al. (2008) Until recently, the diagnosis of P. cinnamomi as the provides a recent and comprehensive review discussing causative agent of disease required laboratory analysis the potential for employing predictive mapping for of samples of soil and tissues from affected plants. The P. cinnamomi. majority of laboratories in Australia with the capacity to analyse samples for the presence of P. cinnamomi Various attempts at mapping have been made using have used conventional identification of technological methods, such as satellite imagery; morphological characteristics, primarily of the however, the success of using these methods has been characteristic hyphae and reproductive structures constrained by the nature of the impact of (Drenth and Sendall, 2001, cited in O’Gara et al., P. cinnamomi which is often restricted in visual 2005a). impact. Maps produced from the interpretation of aerial photographs do not have the same level of PCR-based methods should help to facilitate the accuracy or detail as those produced by on-ground identification of further vulnerable plant species and surveys. are expected to improve the economic feasibility of both the sampling to detect, or confirm visible Hill et al. (2009) demonstrated the ability of digital evidence of infection. This should assist in the multi-spectral imaging to determine disease extent subsequent mapping of infested sites and the over broad areas in P. cinnamomi -infested heathland continued monitoring of disease fronts. communities in southern Victoria. In this situation, symptoms of P. cinnamomi arise as a mosaic within healthy vegetation. The study found that digital 3.1.3 Mapping multi-spectral imaging, derived from light aircraft The current distribution of P. cinnamomi in Australia survey, provides a non-invasive, cost-effective tool for is not well known. Direct mapping, involving management of Victorian heathland. on-ground survey, is impractical due to high costs and To improve the chance of finding P. cinnamomi in the the difficulties associated with sampling. Furthermore, Greater Blue Mountains World Heritage Area, species the autonomous movement and spread of the distribution modelling using information about pathogen by uncontrolled vectors means that P. cinnamomi ecology was undertaken. This was then P. cinnamomi distribution maps have a limited used to identify the parts of the landscape where currency of one to three years. P. cinnamomi was most likely to be, prior to Up-to-date maps that accurately depict the boundaries conducting sampling. New models to predict the between infected and uninfected sites assist with both distribution of P. cinnamomi with a very high level of determining where the pathogen is and where it may accuracy were developed. This also allowed the go. This informs on-ground management and assists identification of environmental variables (for example with mitigation of the impact of disease. The costs of rainfall, temperature etc.) that significantly influence on-ground survey and sample analyses have made the the distribution of the organism. This approach can initial mapping or updating of maps expensive and reduce the area to be sampled and increase the chances only applicable ahead of major operations requiring of successfully finding the pathogen (Newby, 2013).

15 3.2 Minimising the spread of For sound management of access to uninfected areas, it is necessary to delineate the boundaries between Phytophthora cinnamomi infected and uninfected areas. A number of elements In the absence of any fully tested and effective that are essential to operational planning include: mechanism to eradicate the pathogen from an area, • recognition of the boundaries between infected and the primary objective of disease management is to uninfected areas protect the biodiversity of areas which, in the long term, are at risk from dieback caused by P. cinnamomi. • mapping of the boundaries between the two areas as ‘Protectable areas’ are defined as uninfected areas, a basis for future access occurring in the vulnerable zone, that have good • demarcation of the boundaries on the ground, so prospects of remaining uninfected over the next two that machinery operators are forewarned and avoid to three decades. crossing into infected areas

The process initially involves the identification of • regular inspection to ensure that entry controls are significant disease-free areas, followed by a risk analysis being followed to determine the probability of the introduction of • regular testing to ensure that the disease has not P. cinnamomi, the identification of potential routes of spread past the boundaries put in place invasion and the manageability of those risks. As humans are the most significant vector of • assessment of the efficacy of controls. P. cinnamomi, managing spread predominantly Difficulties with these sorts of quarantine measures can involves the modification of human behaviours and arise for social and resource-related reasons, such as: activities. • opposition to changes in land use/access • level of public education required 3.2.1 Access prohibition or restriction • lack of resources necessary to enforce quarantine and hygiene processes. Prohibiting access or quarantining an area is generally used to protect biodiversity assets of high conservation value from P. cinnamomi. Prohibition of access may be 3.2.2 Hygiene enforceable under legislation, for example, the Where access is permitted, hygiene refers to specific Western Australian Conservation and Land procedures designed to prevent the spread of Management Act 1984, the South Australian National P. cinnamomi by ensuring that infected soil, water and/ Parks and Wildlife Act 1972, the Tasmanian Plant or plant material are removed from machinery, vehicles, Quarantine Act 1997 and the New South Wales equipment and footwear before entering uninfected National Parks and Wildlife Act 1974. areas. Management options include: As P. cinnamomi can be readily spread in infected soil, • postponing activities during wet weather plant material and water, access to specified areas may be restricted to periods when soils are not likely to • beginning activities with clean vehicles and adhere to vehicles and pedestrians or when the equipment likelihood of pathogen transmission is low. Land • avoiding wet or muddy areas during activities managers may choose to restrict all access or just • leaving heavy equipment in infected area where they vehicular traffic. Recreational activities such as are regularly used. bushwalking, cycling and horse-riding are perceived in some areas and under some circumstances to pose a Permanent or semi-permanent vehicle wash-down low risk and may be allowable under specific facilities may be constructed where machinery and conditions. vehicles require routine cleaning for fixed activities. Portable wash-down systems enable machinery, vehicles

16 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi and any item that comes into contact with the ground, encouraging park visitors to use them in order to to be cleaned at the point of risk for activities that do protect large areas of susceptible vegetation on high not have a fixed location. profile walking tracks such as the Frenchman’s Cap track. While they are a useful tool to minimise risks to Where high conservation values are at stake, activities priority areas, there are difficulties associated with the such as bushwalking, horse riding and cycling may implementation of hygiene measures to ensure the pose a risk of introduction and may also be subject to optimal uptake of and compliance with these hygiene. Disinfection of footwear, small tools and measures. equipment against P. cinnamomi is required to maintain disease-free status in these instances.

The specific difficulties associated with maintaining 3.2.3 Potential further introductions the integrity of the boundary between infected and through revegetation uninfected areas include: P. cinnamomi occurs in the nursery and garden industry, where the pathogen can kill potted plants • access to suppress wildfires and for installing and and infest plant growth medium. The use of infected maintaining firebreaks on private property plant stock has the potential to spread the disease boundaries extensively in urban and rural situations and may • denial of access to uninfected areas when wet soils become problematic when gardens or rehabilitation are likely to be picked up from cryptic infections activities adjoin natural bushland. Many consumers in timber-harvesting coupes and spread further are unaware of the threat posed by purchasing plants within the coupes (this results in the need to and plant medium and introducing P. cinnamomi into stockpile timber produce during drier periods in the natural environment. Consumers are also unaware order to limit movement of infected mud) that this threat can be minimised by purchasing these • mapping and demarcation in planning access for from certified sources. heavy equipment, to minimise the inadvertent Revegetation of much of the landscape is occurring on movement of machinery from uninfected areas a broad scale across the vulnerable envelope for into infected ones and vice versa P. cinnamomi and the threat of continued spread of • access for other activities, for example bush P. cinnamomi from infected stock and nurseries is walking, apiarian, drilling, wildflower collecting. potentially significant. A key objective for much of the revegetation work is to enhance or restore the The Dieback Working Group (WA) has produced landscape; however, this may be nullified if Managing Phytophthora dieback in bushland—a guide P. cinnamomi is introduced in the process. Managing for landholders and community conservation groups the threat will require targeting both producers and (Edition 4, 2008). In addition, the Tasmanian consumers of products. Government publication Keeping it clean (Allan and Gartenstein 2010) and the NSW Government’s Clean Nurseries in many states have voluntary best-practice & Healthy Programme (OEH, forthcoming) provides guidelines to reduce the spread of P. cinnamomi via thorough hygiene related methodologies to minimise infected stock. The Nursery and Garden Industry of the risk of introduction or spread of exotic diseases Australia (NGIA) supports the Nursery Industry into state managed lands. These documents include Accreditation Scheme (NIASA). The NIASA is a disinfection and cleaning processes for many activities, national scheme for production nurseries, growers, including the use of vehicles and heavy machinery; fire growing media and potting mix businesses which fighting; movement of infected gravel, sand, soil or operate in accordance with a set of national ‘best water during road construction and maintenance. As practice’ guidelines. Further information is at the an example of the implementation of such hygiene NGIA website: www.ngia.com.au. prescriptions, the Tasmanian Parks and Wildlife Service is providing wash down stations and

17 3.2.4 Eradication Currently there are scant data available on the A method for eradicating small infestations of effectiveness of current management tactics, P. cinnamomi has been developed and could be applied particularly hygiene measures, due to insufficient in suitable areas where high value biodiversity assets monitoring. occur. The process involves a sequence of treatments: vegetation (host) destruction, fungicide and fumigant treatments, and containment barriers to protect 3.3 Treatment options to threatened vegetation (Dunstan et al., 2010; mitigate the impact of Dunne et al., 2011). Phytophthora cinnamomi Dunstan et al. (2010) applied increasingly robust treatments including vegetation (host) destruction, Options for the mitigation of impact to biodiversity at fungicides, fumigation and physical root barriers at infected sites are currently limited to the use of the two P. cinnamomi infested sites with differing climate fungistatic agent phosphite. Ex situ conservation of and vegetation types. P. cinnamomi was not recovered susceptible plants is a management option for the at three assessments of treated plots 6 to 9 months preservation of susceptible and rare plants. The cost of after treatments. these options makes only limited application practical and as a result in situ conservation is more often the approach taken by land managers dealing with 3.2.5 Monitoring and surveillance P. cinnamomi. The breeding of resistant plants such as Effective monitoring and surveillance for the presence E. marginata (jarrah), while expensive, is another of P. cinnamomi is essential to allow timely option for the rehabilitation of high priority infected management. sites (see section 3.3.4).

Monitoring and surveillance of plant communities provides information on disease outbreaks, as well as 3.3.1 Phosphite on distribution, prevalence and incidence of The autonomous spread of P. cinnamomi is currently P. cinnamomi. It also provides information necessary impossible to control. However, phosphite (also for evaluating the risk P. cinnamomi poses to referred to as phosphonate), the anionic form of biodiversity and the effectiveness and efficiency of 2- phosphonic acid (HPO3 ), has been shown in management and risk mitigation measures. Western Australia and Victoria to slow the spread and P. cinnamomi The purpose of monitoring ranges from determining reduce the impact of in susceptible long-term patterns of pathogen spread and disease vegetation. Phosphite exhibits a complex mode of impact, to determining the effectiveness of action, both acting directly on the pathogen and management measures and/or surveillance of pathogen indirectly by stimulating host defence responses to movement where high conservation values are under inhibit pathogen growth. imminent threat. Surveys can be one-off to determine Phosphite is currently used in Western Australia to if a site is infected with the pathogen, or they can be protect areas of high conservation value and critically systematic and ongoing. Systematic ongoing surveys endangered species from the threat of P. cinnamomi. focused on key sites provide data on the epidemiology of the disease over time. Information about pathogen Phosphite is potentially applicable in a national occurrence, susceptible species, climate and context and, given limited management options, topography can be employed to develop predictive provides states and territories with an important tool. maps for potential future occurrence and risk of It should however, be used judiciously, with reference introduction of the disease. to available research and close monitoring of results. This will build the body of knowledge relating to the effectiveness of this form of management.

18 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi The beneficial properties of phosphite include: communities. Due to these unknown factors, a considered approach needs to be adopted when using • the induction of resistance to P. cinnamomi in phosphite for the management of P. cinnamomi in otherwise susceptible plant species (Guest and natural ecosystems. Bompeix, 1990) The Australian Pesticides and Veterinary Medicines • its mobility in phloem and xylem (enabling Authority (APVMA) administer the National application by stem injection to trees and Registration Scheme for Agricultural and Veterinary large shrubs Chemicals in partnership with the states and • its uptake through foliage which enables it to be territories. Phosphite is currently not registered for use applied as a foliar spray, either manually or by in native vegetation and therefore an ‘off-label permit’ broad scale aerial application is required from the APVMA before use. However, as • its quick break down in the soil (Guest and Grant, legislation can vary between states/territories it is 1991, cited in O’Gara et al., 2005a). recommended that the APVMA or the relevant APVMA state/territory co-ordinator is contacted for Phosphite has a low toxicity for many mammals, advice on permit requirements before use. although its effects on other fauna have not yet been properly assessed. The chemical should be used as Aerial application (figure 3) is a rapid way to treat regulated and with caution in areas where threatened entire plant communities especially where rough fauna species are known to occur. terrain would make ground application practically impossible or prohibitively expensive. Foliar The detrimental effects of phosphite on non-target application using backpack (figure 4) or trailer- species may include phytotoxicity, growth mounted sprayers is usually restricted to small areas abnormalities and reduced reproductive capability in such as small reserves, remnant bushland or spot some species (Hardy et al., 2001). infections. Trunk injection of trees and large shrubs is used in strategic areas where their loss would have a There are also large differences in levels of control high visible impact and where foliar application is between plant species. In addition, phosphite is not an impractical. Bark painting may also be effective; eradicant and the pathogen remains in the soil/host techniques need to be further developed for this plant environment even though symptoms are method. suppressed. Moreover, there is emerging research that indicates that long term phosphite application may cause the accumulation of phosphate levels in the soil. This might cause the decline or modification of plant

19 Figure 3 Aerial application of phosphite Figure 4 Foliar application of phosphite in Stirling Ranges National Park in the by backpack mister south-west of Western Australia (Photo: B Shearer, Department of Parks and Wildlife, Western Australia). (Photo: G Freebury, Department of Parks and Wildlife, Western Australia).

The cost of phosphite application precludes broad scale application to infected sites. The use of phosphite plants spreading P. cinnamomi through and/or ex situ conservation as a component of root-to-root transmission was installed. The integrated management for a site or area requires a fungicide metham sodium was applied through process of prioritisation and strategic planning. a subterranean irrigation system at the location Highest priority may be given to sites assessed as of the root-impervious membrane to increase ecologically or economically significant, or valued by the potential to contain the pathogen. The the community. fungicide phosphite was aerially and ground applied to part of the 375 hectares of the Fitzgerald River National Park within the Case study: Prevention of spread in Bell Track project area. WA DEC contained this infestation, protecting the largely disease free the Fitzgerald River National Park, WA status of the rest of Fitzgerald River National In Western Australia, the Department of Park. The process has been published in the Environment and Conservation (WA DEC) New Zealand Journal of Forestry Science and conducted a large scale containment project on could be used as the basis for similar work in an infestation within an internally draining appropriate locations (Dunne et al., 2011). catchment in Fitzgerald River National Park. A Bayesian Belief Network model was developed for the range of management strategies and their effect on containment of the P. cinnamomi 3.3.2 Ex situ conservation infestation. WA DEC constructed a Ex situ conservation of germplasm in seed banks is a 12 kilometre fence around the entire Bell Track well established technique and with no definitive infestation to prevent people and animals solution to the threat of P. cinnamomi, it may be the spreading the disease. In 2008, a three- last hope in conserving some susceptible species. kilometre-long plastic membrane to prevent Compared to other types of germplasm, seed conservation has many benefits, including the simplicity of the technology, low cost and space

20 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi requirements, the potential for long-term storage with in Western Australia selecting for resistance of little loss of seed viability, the applicability of the E. marginata to P. cinnamomi. This breeding program technique to a wide range of species and greater has particular but limited application for forestry and genetic representation in seed than in vegetative rehabilitation of infected sites in the E. marginata material (Cochrane, 2004). forest.

The work of the Australian Seed Bank Partnership There have been very real gains made in dieback- (ASBP) is a national effort to conserve Australia’s affected forests in Victoria following the use, for over native plant diversity through collaborative and 30 years, of a strategy to exploit the potential that a sustainable seed collecting, banking, research and small percentage of individuals of otherwise knowledge sharing. Seed banking is a principal tool susceptible species are tolerant (Marks and Smith, for the safe and efficient storage of wild plant genetic 1991). Sites have been successfully rehabilitated diversity, and provides a resource and knowledge base through the strategy of sowing well prepared seedbeds to support the management and conservation of plant with high numbers of seeds collected from trees species and communities in Australia (ASBP website). endemic to the sites. While the resilience of the apparent resistance seen is still to be proven, the outcome to date is that the percentage that survives 3.3.3 In situ conservation more than provides for an adequate restocking of Translocation is the deliberate transfer of plants or eucalypts on these previously dieback-affected sites. regenerative plant material from one place to another. This approach also ensures that the stocking rate is Purposes for translocation include (Vallee et al., 2004): high enough to potentially lower the water table and thus reduce conditions conducive to disease • enhancement—an attempt to increase population development. size or genetic diversity by adding individuals to an existing population A program for breeding resistant individuals of susceptible keystone or threatened species, if proven • re-introduction—the establishment of a practical, could provide a basis for rehabilitation of population in a site where it formerly occurred sites affected by the disease. • conservation introduction—an attempt to establish a taxon at a site where it is not known to occur now or to have occurred in historical times, 3.3.5 Other methods of control but which is considered to provide appropriate Soil microorganisms have been shown to be effective habitat for the taxon. controls for Phytophthora in experimental conditions (El-Tarabily et al., 1996). The potential use of Guidelines for the translocation of threatened plants biocontrol agents to mitigate spread and impact of in Australia (Vallee et al., 2004) take into account the Phytophthora could present as a more sustainable and benefits, risks, planning and implementation effective approach to managing this threat in the associated with the strategy. long term.

3.3.4 Breeding for resistance There may be considerable variation in the expression of disease within a species. It has been observed that remaining and apparently healthy E. marginata (jarrah) in diseased jarrah forest are often the resistant component. Intra-specific resistance has been demonstrated using clones of susceptible E. marginata (Stukely and Crane, 1994) and the resistant individuals are the basis of a plant breeding program

21 3.4 Wide scale detection, The criteria used to identify zones of vulnerability vary diagnosis and from state to state. demarcation protocols A risk assessment process has been developed for assessing the risk of P. cinnamomi to threatened In order to survey and map the distribution of species, ecological communities and areas, and ranking P. cinnamomi on a wide scale, a uniform and them as the basis for setting management priorities. consistent sampling standard for application across the This is potentially suitable for national adoption country is required. The presence of P. cinnamomi at a (CPSM 2005). Models have been developed for flora, site can be confirmed from a single positive sample fauna habitat, vegetation communities and for areas but a site cannot be deemed free of the pathogen from of land. a single or even multiple negative samples. The models identify the source of risk, the likelihood A systematic survey of long-infected sites in Western of occurrence and the magnitude of the consequences. Australia determined that the number of samples The models are semi-quantitative (i.e. qualitative needed to return a negative result to pronounce a site criteria are assigned scores), based on current scientific free of P. cinnamomi with 95 per cent confidence, knowledge. However, where significant knowledge or is 271 (Davison and Tay 2003, cited in O’Gara et al., data gaps exist, expert opinion will be required. The 2005a). semi-quantitative scoring system used in developing the models enabled a ranking of assets according to In the wet tropics of northern Queensland, the risk posed by P. cinnamomi and the perceived P. cinnamomi was shown to be uniformly distributed ability to manage the risks. Indicative assessments are in the landscape and it was estimated that a minimum produced when the models are run. The decision flow 2 of two to four soil samples were required per 1256m chart contained in the model terminates with the to predict the absence of P. cinnamomi with determination of disease status of the site, with three

95 per cent confidence (Pryce et al., 2001, cited in possible options: infected, uninfected or disease status O’Gara et al., 2005a). unknown.

The European and Mediterranean Plant Protection Barrett et al. (2008) drew on this risk assessment Organisation has produced a standard for application methodology in a species risk assessment model for in that region that describes diagnostic protocols for the rare flora of the South Coast of Western Australia. P. cinnamomi including examination of symptoms, isolation, identification of the pathogen through Major P. cinnamomi containment work undertaken at morphological characteristics, immunological and the Bell Track site in Fitzgerald National Park used a molecular methods and reporting (OEPP/EPPO Bayesian based risk model to assess the risks associated 2004). with the project (C Dunne [WA DEC] 2011, pers. comm.).

Within the Wet Tropics, a preliminary risk assessment 3.5 Risk assessment and methodology has been developed that guides decisions priority setting concerning implementation of hygiene measures during operational works. Studies have identified high, One of the first steps in the analysis of the risk posed moderate and low risk zones within the World by P. cinnamomi is the identification of areas Heritage Area (Worboys and Gadek, 2004). vulnerable to disease. Most states in Australia have Implementation of hygiene measures is recommended identified broad zones where biodiversity is vulnerable for works within high and moderate risk zones in to the threat of P. cinnamomi due to the coincidence of order to prevent transfer of the pathogen from infested susceptible vegetation and environmental conditions catchments. that are conducive to the establishment and persistence of the pathogen (see section 2.2.3).

22 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi A more recent approach (2012) to risk management is In New South Wales, Keith et al. (2011) assessed the that taken by the Victorian Department of P. cinnamomi threat to Royal National Park through Environment and Primary Industries (Vic DEPI). Vic modelling the probability of infection as a function of DEPI has used known sites of impact to produce a environmental variables (soil, landscape, topographic Species Distribution Model (SDM) for P. cinnamomi. position, aspect and slope) and mapping plant This model factors in relevant climate and terrain communities in which susceptible species are most variables and may be used to determine the risk to abundant. This data provided maps showing the risk individual taxa. To determine the risk to vegetation of plant diversity loss to P. cinnamomi. communities Vic DEPI combined the P. cinnamomi Information regarding the susceptibility of threatened SDM with a vegetation impact model to produce a plant species in South Australia is very limited. A risk risk map showing the relative risk of impact across assessment based on status and proximity to Victoria. Vic DEPI Intends to make this information P. cinnamomi infestations was developed to prioritise available via the web to land managers along with threatened plant species for research and management guidelines for P. cinnamomi management. The risk options (Velzeboer et al., 2005). map can be reviewed at different scales and allows for rapid local area management decisions and preparation The risk assessment process developed should be of local area plans. viewed as iterative, and improvements and reviews undertaken as new data and knowledge become Similarly, Tasmania has undertaken a project which available. established a set of priority areas for management of P. cinnamomi for threatened species and ecological communities that are at risk from P. cinnamomi (Schahinger et al., 2003). This document rated vegetation community susceptibility due to frequency of susceptible species and environmental susceptibility. The largest disease-free areas or areas most manageable (considering factors such as disease proximity, landscape features and ease of access etc.) were selected for priority management. A regional plan for the management of P. cinnamomi in the Tasmanian Wilderness World Heritage Area has been developed which addresses biodiversity assets at risk and identifies large disease-free areas.

23 References

Aberton MJ, Wilson BA, Hill J & Cahill DM 2001, Cochrane A, Barrett S, Crane C, Dunne C, Hartley R ‘Development of disease caused by Phytophthora & Freebury G 2011, ‘Last chance to see: cinnamomi in mature Xanthorrhoea australis’, of the south coast of Western Australia’, Landscope, Australian Journal of Botany, vol. 49, pp. 1–11. vol. 26(4), pp. 17–22.

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ANPC—see Australian Network for Plant Commonwealth Scientific and Industrial Research Conservation. Organisation (CSIRO), Australian Bureau of Meteorology 2007, Climate change in Australia— ASBP—see Australian Seed Bank Partnership . climatechangeinaustralia.gov.au>. Barrett S, Shearer BL, Crane CE & Cochrane A 2008, Commonwealth Scientific and Industrial Research ‘An extinction-risk assessment tool for flora Organisation (CSIRO), Australian Bureau of threatened by Phytophthora cinnamomi’, Australian Meteorology 2012, State of the climate 2012, Journal of Botany, vol. 56(6), pp. 477–486. . Cahill DM, Rookes JE, Wilson BA, Gibson L CPSM—see Centre for Phytophthora Science and & McDougall KL 2008, ‘Phytophthora cinnamomi Management. and Australia’s biodiversity: impacts, predictions and progress towards control’, Turner Review Crone M, McComb JA, O’Brien PA & Hardy GEStJ no. 17, Australian Journal of Botany, vol. 56(4), 2012, ‘Annual and herbaceous perennial native pp. 279–310. Australian plant species are asymptomatic hosts of Phytophthora cinnamomi on black gravel sites in Calver MC & Dell J 1998, ‘Conservation status of the Eucalyptus marginata (jarrah) forest of Western mammals and birds in south-western Australian Australia’, Plant Pathology, vol. 62(5), pp. 1057– forests: Is there evidence of direct links between 1062. forestry practices and species decline and extinction?’ Pacific Conservation Biology, vol. 4, Crone M, McComb JA, O’Brien PA & Hardy GEStJ pp. 296–314. 2013, ‘Survival of Phytophthora cinnamomi as oospores, stromata and thick walled Centre for Phytophthora Science and Management chlamydospores in roots of symptomatic and (CPSM) 2005, Management of Phytophthora asymptomatic annual and herbaceous perennial cinnamomi for biodiversity conservation in Australia: plant species’, Fungal Biology, vol. 117(2), Part 4—Risk assessment models for species, ecological pp. 112–123. communities and areas, a report funded by the Commonwealth Government Department of the CSIRO—see Commonwealth Scientific and Industrial Environment and Heritage by the Centre for Research Organisation. Phytophthora Science and Management, Murdoch University, Western Australia.

24 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi Davison EM & Tay FCS 2003, A sampling strategy for Environment Australia 2001, Threat abatement plan Phytophthora for ‘difficult’ sites Report no. 235, for dieback caused by the root-rot fungus Minerals & Energy Research Institute of Western Phytophthora cinnamomi, Environment Australia, Australia, East Perth. Commonwealth Government of Australia, Canberra. Department of Conservation and Land Management (WA) 2003, Phytophthora cinnamomi and disease European and Mediterranean Plant Protection caused by it, Department of Conservation and Land Organisation 2004, ‘Diagnostic protocols for Management, Government of Western Australia, regulated pests’, Bulletin OEPP/EPPO, vol. 34, . information-sheets.html>. Friend JA 2004, Dibbler recovery plan July 2003 – Department of the Environment 2014, Threat abatement June 2013, Western Australian Wildlife plan for disease in natural ecosystems caused by Management Program No 38, Department of Phytophthora cinnamomi, Commonwealth Conservation and Land Management, Perth, Government of Australia, Canberra, p. 26, . threatened-species-ecological-communities/threat- Gadek PA & Worboys S 2003, Rainforest dieback abatement-plans/approved-threat>. mapping and assessment: Phytophthora species Drenth A & Sendall B 2001, Practical guide to detection diversity and impacts of dieback on rainforest and identification of Phytophthora, Cooperative canopies, Cooperative Research Centre for Tropical Research Centre for Tropical Plant Protection, Rainforest Ecology and Management, Cairns, Brisbane, Australia. Queensland p. 114.

Dunne C, Crane CE, Lee M, Massenbauer T, Barrett S, Gates JA 2011, Recovery plan for the Kangaroo Island Comer S, Freebury GJC, Utber DJ, Grant MJ & Dunnart (Sminthopsis atkeni), Department of Shearer BL 2011, ‘A review of the catchment Environment and Natural Resources, South approach techniques used to manage a Phytophthora Australia, p. 23, . coast of Western Australia’, New Zealand Journal of Garavanta CAM, Wooller RD, Richardson KC 2000, Forestry Science, vol. 41, pp. S121–S132, ‘Movement patterns of honey possums, Tarsipes . pp. 179–183. Dunstan WA, Rudman T, Shearer BL, Moore NA, Global Invasive Species Database, . ‘Containment and spot eradication of a highly destructive, invasive plant pathogen (Phytophthora Guest DI & Bompeix G 1990, ‘The complex mode of cinnamomi) in natural ecosystems’, Biological action of phosphonates as antifungal agents’ Invasions, vol. 12(4), pp. 913–925. Australasian Plant Pathology, vol. 19, pp. 113–115.

El-Tarabily KA, Sykes ML, Kurtböke ID, Hardy GEStJ, Guest DI & Grant B 1991, ‘The complex action of Barbosa AM & Dekker RFH 1996, ‘Synergistic phosphonates as antifungal agents’, Biological effects of a cellulase-producing Micromonospora Reviews, vol. 66, pp. 159–187. carbonacea and an antibiotic-producing Streptomyces violascens on the suppression of Phytophthora Hardham AR 2005, ‘Phytophthora cinnamomi’, cinnamomi root rot of ’, Canadian Molecular Plant Pathology vol. 6, pp. 589–604. Journal of Botany, vol. 74(4), pp. 618–624.

25 Hardham AR 1999, ‘Cell biology of Phytophthora Menkhorst P & Broome L 2006, National recovery cinnamomi’, in Gadek PA (ed), Patch deaths in plan for the smoky mouse Pseudomys fumeus, State of tropical Queensland rainforests: association and Victoria Department of Sustainability and impact of Phytophthora cinnamomi and other soil Environment, Melbourne, p. 19, . Management, Cairns, Queensland. Newby Z 2013, Quantifying the risk of Phytophthora Hardy GEStJ, Barrett S & Shearer BL 2001, ‘The dieback in the Greater Blue Mountains World future of phosphite as a fungicide to control the Heritage Area, unpublished PhD thesis, The soil borne plant pathogen Phytophthora cinnamomi University of Sydney and the Royal Botanic in natural ecosystems’, Australasian Plant Gardens and Domain Trust, Sydney. Pathology, vol. 30, pp. 133–139. Newell GR & Wilson BA, 1993, ‘The relationship Hill TCJ, Tippett JT & Shearer BL 1995, ‘Evaluation between Cinnamon fungus (Phytophthora of three treatments for eradication of Phytophthora cinnamomi) and the abundance of Antechinus cinnamomi from deep, leached sands in southwest stuartii (Dasyurida: Marsupialia) in the Brisbane Australia’, Plant Disease, vol. 79, pp. 122–127. Ranges, Victoria’, Wildlife Research, vol. 20, pp. 251–259. Hill RJ, Wilson BA, Rookes JE & Cahill DM 2009, ‘Use of high resolution digital multi-spectral O’Brien PA 2008, ‘PCA primers for specific detection imagery to assess the distribution of disease caused of Phytophthora cinnamomi’, Australasian Plant by Phytophthora cinnamomi on heathland at Pathology, vol. 37, pp. 69–71. Anglesea, Victoria’, Australasian Plant Pathology, OEH—see Office of Environment and Heritage, vol. 38, pp. 110–119. Government of New South Wales. Keith DA, McDougall KL, Simpson CC & Walsh J OEPP—see European and Mediterranean Plant 2011, ‘Spatial analysis of risks posed by root-rot Protection Organisation. pathogen, Phytophthora cinnamomi: Implications for disease management’, Proceedings of the Linnean Office of Environment and Heritage, Government of Society of New South Wales, vol. 134, pp. 147–179. New South Wales, Clean & Healthy Programme, forthcoming. Laidlaw WS & Wilson BA 2006, ‘Habitat utilisation by small mammals in a coastal heathland O’Gara E, Howard K, Wilson B & Hardy GEStJ exhibiting symptoms of Phytophthora cinnamomi 2005a, Management of Phytophthora cinnamomi infestations’, Wildlife Research, vol. 33, for biodiversity conservation in Australia: Part 1— pp. 639–649. A review of current management, a report funded by the Commonwealth Government Department of Lucas A 2003, Water stress and disease development in the Environment and Heritage by the Centre for Eucalyptus marginata (jarrah) infected with Phytophthora Science and Management (CPSM), Phytophthora cinnamomi, thesis presented for the Murdoch University, Western Australia. degree of Doctor of Philosophy in the Department of Biological Sciences, Murdoch University, Perth, O’Gara E, Howard K, Wilson B & Hardy GEStJ Western Australia, p. 235 . biodiversity conservation in Australia: Part 2— National best practice guidelines, a report funded by Marks GC & Smith IW 1991, ‘The cinnamon fungus the Commonwealth Government Department of in Victorian forests; History, distribution, the Environment and Heritage by the Centre for management and control’ Lands and Forests Phytophthora Science and Management, Murdoch Bulletin no. 31, Department of Conservation and University, Western Australia. Environment, Melbourne, p. 33.

26 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi Ouimette DG & Coffey MD 1990, ‘Symplastic entry Strelein GJ, Sage LW & Blankendaal PA 2006, ‘Rates and phloem translocation of phosphonate’, of disease extension of Phytophthora cinnamomi in Pesticide Biochemistry and Physiology, vol. 38, the jarrah forest bioregion of southwestern pp. 18–25. Australia’ in Brasier C, Jung T & Oswald W (eds), Progress in research on Phytophthora diseases of forest Podger FD, James SH & Mulcahy MJ 1996, Review of trees: Proceedings of the 3rd International Union of dieback in Western Australia, vol. 1, Report and Forest Research Organizations (IUFRO) working recommendations, report to the Western Australian party S07.02.09 meeting, Freising, Germany, Minister for the Environment, Perth, Western 11–18 September 2004, pp. 49–52, Forest Australia. Research, Farnham, UK. Phytophthora Technical Group 2006, Phytophthora Stukely MJC & Crane CE 1994, ‘Genetically based management guidelines, 2nd edn, Government of resistance of Eucalyptus marginata to Phytophthora South Australia, . Vallee L, Hogbin T, Monks L, Makinson B, Matthes M & Rossetto M 2004, Guidelines for the Pryce J, Edwards W & Gadek P 2001, ‘Detecting translocation of threatened plants in Australia, 2nd Phytophthora cinnamomi in rainforest soils: the edn, Australian Network for Plant Conservation, effect of spatial scale on sampling strategy’, in Canberra, p. 80, . & Pryce J (eds), Rainforest dieback mapping and assessment in the Wet Tropics World Heritage Area, Velzeboer R, Stubbs W, West A & Bond A 2005, James Cook University (Cairns campus) and Threatened plant species at risk from Phytophthora in Cooperative Research Centre for Tropical South Australia, Department for Environment and Rainforest Ecology and Management. Heritage, Adelaide, p. 35.

Rands R 1922, Streepkanker van kaneel, veroorzaakt Weste G & Ashton DH 1994, ‘Regeneration and door Phytophthora cinnamomi n. sp. (Stripe canker survival of indigenous dry sclerophyll species in of cinnamon, caused by Phytophthora cinnamomi the Brisbane Ranges, Victoria, after a Phytophthora n. sp), Mededelingen van het Instituut voor cinnamomi epidemic’, Australian Journal of Botany, Plantenziekten 54, Ruygrok, Batavia (Jakarta). vol. 42, pp. 239–253.

Schahinger R, Rudman T & Wardlaw T 2003, Weste G, Brown K, Kennedy J & Walshe T 2002, Conservation of Tasmanian plant species and ‘Phytophthora cinnamomi infestation—a 24 year communities threatened by Phytophthora cinnamomi: study of vegetation change in forests and Strategic regional plan for Tasmania, Technical woodlands of the Grampians, Western Victoria’ Report 03/03, Nature Conservation Branch, Australian Journal of Botany, vol. 50, pp. 247–274. Department of Primary Industries, Water and Williams N, Hardy GEStJ & O’Brien PA 2009, Environment (DPIWE), Hobart. ‘Analysis of the distribution of Phytophthora Shearer BL, Crane CE & Cochrane A 2004, cinnamomi in soil at a disease site in Western ‘Quantification of the susceptibility of the native Australia using nested PCR’, Forest Pathology, vol. flora of the South West Botanical Province, 39(2), pp. 95–109. Western Australia, to Phytophthora cinnamomi’, Wills RT 1993, ‘The ecological impact of Phytophthora Australian Journal of Botany, vol. 52(4), cinnamomi in the Stirling Range National Park, pp. 435–443. Western Australia’, Australian Journal of Ecology, vol. 18, pp. 145–159.

27 Wilson BA, Howard K, O’Gara E & Hardy GEStJ Wilson BA, Newell G, Laidlaw WS & Friend G 1994, 2005, Management of Phytophthora cinnamomi for ‘Impact of plant diseases on faunal communities’, biodiversity conservation in Australia: Part 3—Risk Journal of the Royal Society of Western Australia, assessment for threats to ecosystems, species and vol. 77, pp. 139–143. communities: A review, a report funded by the Wooller RD, Richardson KC, Garavanta CAM, Commonwealth Government Department of the Saffer VM & Bryant KA 2000, ‘Opportunistic Environment and Heritage by the Centre for breeding in the polyandrous honey possum, Phytophthora Science and Management (CPSM), Tarsipes rostratus’, Australian Journal of Zoology, Murdoch University, Western Australia. vol. 48, pp. 669–680. Wilson BA & Laidlaw WS 2001, ‘Impact of Worboys S, Gadek P 2004, Rainforest dieback: risks Phytophthora cinnamomi on mammals in southern associated with roads and walking tracks, Australia’, Phytophthora in forests and natural Cooperative Research Centre for Tropical ecosystems: Proceedings of the 2nd International Union Rainforest Ecology and Management, Cairns, of Forest Research Organizations (IUFRO) Working Queensland. Party 7.02.09 Meeting, Albany, Western Australia, 30 September – 5 October 2001, Murdoch University Print, Murdoch, Western Australia.

Wilson BA, Lewis A & Aberton J 1997, Conservation of national estate communities threatened by cinnamon fungus at Anglesea, Victoria, Report for the Victorian Government Department of Natural Resources and Environment, Melbourne, p. 93.

28 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi Appendix A

Data contributions for figure 2 Organisations Papers ACT Parks, Conservation and Lands, Australian Brown BN, 1976 ‘Phytophthora cinnamomi associated Capital Territory (2011) with patch death in tropical rain forests in Queensland’, Australian Plant Pathology Society Deakin University, Melbourne, Victoria Newsletter, vol. 5(1), pp. 1–4. Department of Environment and Primary Industry, Victoria (2011)

Department of Primary Industries, Parks, Water and Environment, Tasmania (2010)

Department of Environment and Natural Resources, South Australia (2011)

Department of Environment and Conservation, Western Australia (2011)

Geoscience Australia (2004): Gazetteer of Australia

Geoscience Australia (2003): Australia, TOPO-2.5M Topographic Data

Gondwanana Rainforest of Australia World Heritage Area, Australian Government (2011)

Plant Health Australia (2011)

Royal Botanic Gardens and Domain Trust Sydney, New South Wales (2011)

Wet Tropic Management Authority (2011)

29 Appendix B

Suggested reading Further Reading

O’Gara E, Howard K, Wilson B & Hardy GEStJ Aberton M, Wilson BA & Cahill DM 1999, 2005a, Management of Phytophthora cinnamomi for ‘The use of phosphite as a control for Phytophthora biodiversity conservation in Australia: cinnamomi in native vegetation at Anglesea, Part 1—A review of current management, a report Victoria’, Australasian Plant Pathology, vol. 28, funded by the Commonwealth Government pp. 225–234. Department of the Environment and Heritage by ALCOA 2006, Dieback Management Fact Sheet, Alcoa the Centre for Phytophthora Science and of Australia Limited, Booragoon, Western Management (CPSM), Murdoch University, Australia, O’Gara E, Howard K, Wilson B & Hardy GEStJ Barker PCJ, Wardlaw TJ & Brown MJ 1996, 2005b, Management of Phytophthora cinnamomi for ‘Selection and design of Phytophthora management biodiversity conservation in Australia: Part 2— areas for the conservation of threatened flora in National best practice guidelines, a report funded by Tasmania’, Biological Conservation, vol. 76, the Commonwealth Government Department of pp. 187–193. the Environment and Heritage by the Centre for Phytophthora Science and Management (CPSM), Barrett S, Shearer BL, Crane CE & Cochrane A 2008, Murdoch University, Western Australia. ‘An extinction-risk assessment tool for flora threatened by Phytophthora cinnamomi’, Australian Wilson B, Howard K, O’Gara E & Hardy GEStJ Journal of Botany, vol. 56, pp. 477–486. 2005, Management of Phytophthora cinnamomi for biodiversity conservation in Australia: Part 3—Risk Brasier C 2003, ‘Phytophthoras in European forests: assessment for threats to ecosystems, species and Their rising significance’, Sudden Oak Death communities: A review, a report funded by the Online Symposium, 21 April – 12 May 2003. Commonwealth Government Department of the Environment and Heritage by the Centre for Brown BN 1998, ‘Occurrence and impact of Phytophthora Science and Management (CPSM), Phytophthora cinnamomi and other Phytophthora Murdoch University, Western Australia. species in rainforests of the Wet Tropics World Heritage Area, and of the Mackay region, Please Note: The full reports can be downloaded Queensland’, in Gadek PA (ed), Patch deaths in from: tropical Queensland rainforests: association and borne pathogens, pp. 41–76, Cooperative Research Centre for Tropical Rainforest Ecology and Management, Cairns Queensland.

Colquhoun I & Hardy GEStJ 2000, ‘Managing the risks of Phytophthora root and collar rot during bauxite mining in the Eucalyptus marginata (Jarrah) forest of Western Australia’, Plant Disease, vol. 84(2), pp. 116–127.

30 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi Centre for Phytophthora Science and Management Dieback Working Group 2004, Environmental code of (CPSM) 2013, Climate modelling to determine the practice for the management of phytophthora dieback impacts of Phytophthora cinnamomi under future in extractive industries, Dieback Working Group, climate scenarios, a report funded by the Western Australia, p. 46, . Sustainability, Environment, Water, Population Dunne C, Crane CE, Lee M, Massenbauer T, and Communities by the Centre for Phytophthora Barrett S, Comer S, Freebury GJC, Utber DJ, Science and Management, Murdoch University, Grant MJ & Shearer BL 2011, ‘A review of the Western Australia. catchment approach techniques used to manage a Centre for Phytophthora Science and Management Phytophthora cinnamomi infestation of native plant (CPSM) website, Murdoch University, Western communities of the Fitzgerald River National Park Australia, . on the south coast of Western Australia’, New Zealand Journal of Forestry Science, vol. 41, CPSM - see Centre for Phytophthora Science and pp. S121–S132, . Phytophthora cinnamomi management in Western Dunstan WA, Rudman T, Shearer BL, Moore NA, Australia’, in Calver MC, Bigler-Cole H, Paap T, Calver MC, Dell B & Hardy GEStJ 2010, Bolton G, Dargavel J, Gaynor A, Horwitz P, ‘Containment and spot eradication of a highly Mills J & Wardell-Johnson G (eds), A forest destructive, invasive plant pathogen (Phytophthora consciousness: Proceedings of the 6th Australian Forest cinnamomi) in natural ecosystems’, Biological History Society Conference, Millpress Science Invasions, vol. 12(4), pp. 913–925. Publishers, Rotterdam, Netherlands. Forest Practices Authority 2012, Flora technical note Department for Environment and Heritage 2002, no. 8: Management of Phytophthora cinnamomi in Phytophthora threat management procedure: production forest, Forest Practices Authority, Standard operating procedures 2002, Adelaide, Hobart, Tasmania, p. 16, . Dieback in native vegetation in the Mount Lofty Grant M and Barrett S 2003, ‘The distribution and Ranges: A guide to causes and symptoms, Adelaide, impact of Phytophthora cinnamomi (Rands) in the South Australia, p. 22. south coast region of Western Australia’, in Department of Conservation and Land Management McComb JA, Hardy GEStJ & Tommerup I (eds), (CALM) 2003, Phytophthora cinnamomi and Phytophthora in forests and natural ecosystems: nd disease caused by it, Government of Western Proceedings of the 2 International Union of Forest Australia, Perth. Research Organizations (IUFRO) Working Party 7.02.09 Meeting, Albany, Western Australia, Department of Sustainability and Environment 2005, 30 September – 5 October 2001, Murdoch Draft Strategic Plan for management of Phytophthora University Print, Murdoch, Western Australia. cinnamomi in Victoria, East Melbourne, Australia, p. 31. Hardham AR 1999, ‘Cell biology of Phytophthora cinnamomi’, pp. 27–31, in Gadek PA (ed) Patch Dieback Working Group 2000, Managing deaths in tropical Queensland rainforests: association Phytophthora dieback: Guidelines for local and impact of Phytophthora cinnamomi and other government, Dieback Working Group, Western soil borne organisms, Cooperative Research Centre Australia, p. 95, . Cairns, Queensland.

31 Kilgour S 2000a, Managing Phytophthora dieback in Possingham H, Ryan S, Baxter J & Morton S, 2002, bushland: A guide for landholders and community ‘Setting biodiversity priorities: a paper prepared as conservation groups, 2nd edn, Dieback Working part of the activities of the working group Group, Western Australia. producing the report, Sustaining our natural systems and biodiversity’, Prime Minister’s Science, Leave No Trace Australia website, Leave No Trace Engineering and Innovation Council, Canberra. Australia, Swanbourne, Western Australia . SustainingOurNaturalSystemsAndBiodiversity McDougall KL & Summerell BA 2003, ‘The impact WorkingGroupPaper.pdf> of Phytophthora cinnamomi on the flora and Reiter N, Weste G & Guest D 2004, ‘The risk of vegetation of New South Wales—a re-appraisal’, in extinction resulting from disease caused by McComb JA, Hardy GEStJ & Tommerup I (eds), Phytophthora cinnamomi to endangered, vulnerable Phytophthora in forests and natural ecosystems: or rare species endemic to the Grampians, western Proceedings of the 2nd International Union of Forest Victoria’, Australian Journal of Botany, vol. 52, Research Organizations (IUFRO) Working Party pp. 425–433. 7.02.09 Meeting, Albany, Western Australia, 30 September – 5 October 2001, Murdoch Rudman T 2004, ‘Interim Phytophthora cinnamomi University Print, Murdoch, Western Australia. management guidelines’, Department of Primary Industries, Water and Environment, Government Nursery Industry Accreditation Scheme Australia of Tasmania, Hobart, . in parks’, in National Parks Service, Policy and Shearer BL & Dillon M 1995, ‘Susceptibility of plant Procedures Manual, National Parks Service, species in Eucalyptus marginata forest to infection Department of Conservation and Natural by Phytophthora cinnamomi’, Australian Journal of Resources, Victoria. Botany, vol. 43, pp. 113–134. Pilbeam RA, Colquhoun IJ, Shearer B & Shearer BL & Dillon M 1996, ‘Susceptibility of plant Hardy GEStJ 2000, ‘Phosphite concentration: its species in Banksia woodlands on the Swan Coastal effect on phytotoxicity symptoms and colonisation Plain, Western Australia, to infection by by Phytophthora cinnamomi in three understorey Phytophthora cinnamomi’, Australian Journal of species of Eucalyptus marginata forest’, Australasian Botany, vol. 44, pp. 433–445. Plant Pathology, vol. 29, pp. 86–95. Shearer BL & Tippett JT 1989, ‘Jarrah dieback: The Podger FD 1972, ‘Phytophthora cinnamomi, a cause of dynamics and management of Phytophthora lethal disease in indigenous plant communities in cinnamomi in the Jarrah (Eucalyptus marginata) Western Australia’, Phytopathology, vol. 62, forest of south-western Australia’, Research Bulletin pp. 972–981. no. 3, Department of Conservation and Land Podger FD 1999, A national overview of Phytophthora Management, Government of Western Australia, cinnamomi in Australia: Supplementary information Como, Western Australia, p. 76. to accompany the draft National Threat Abatement Smith I 2002, Guidelines for reducing the spread of Plan, Report prepared for Environment Australia, Phytophthora cinnamomi during earth moving unpublished. operations, Department of Natural Resources and Environment, Government of Victoria, Melbourne.

32 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi Weste G 1974, ‘Phytophthora cinnamomi—the cause of Crous PW, Summerell BA, Shivas RG, Burgess TI, severe disease in certain native communities in Decock CA, Dreyer LL, Granke LL, Guest DI, Victoria’, Australian Journal of Botany, vol. 22, Hardy GEStJ, Hausbeck MK, Hüberli D, Jung T, pp. 1–8. Koukol O, Lennox CL, Liew ECY, Lombard L, McTaggart AR, Pryke JS, Roets F, Saude C, Weste G 1997, ‘The changing status of disease caused Shuttleworth LA, Stukely MJC, Vánky K, by Phytophthora cinnamomi in Victorian open Webster BJ, Windstam ST & Groenewald JZ forests, woodlands and heathlands’, Australasian 2012, ‘Fungal planet description sheets: 107–127’, Plant Pathology, vol. 26, pp. 1–9. Persoonia: Molecular Phylogeny and Evolution of Williams N, O’Gara E, Hardy GEStJ & O’Brien PA Fungi, vol. 28, pp. 138–182. 2009, ‘Development of molecular diagnostic tools Jung T, Stukely MJC, Hardy GEStJ, White D, Paap T, for the detection of Phytophthora cinnamomi from Dunstan WA & Burgess TI 2011, ‘Multiple new cryptic soil samples in southern Australia’, in Phytophthora species from ITS clade 6 associated Phytophthoras in forests and natural ecosystems: with natural ecosystems in Australia: Evolutionary Proceedings of the 4th meeting of the International and ecological implications’, Persoonia: Molecular Union of Forest Research Organizations (IUFRO) Phylogeny and Evolution of Fungi, vol. 26, pp. 13– Working Party S07.02.09, 26–31 August 2007, 39. Monterey, California, p. 348, . Hardy GEStJ, Stukely MJC & Burgess TI 2013, ‘Characterization of Phytophthora hybrids from Wills RT & Keighery GJ 1994, ‘Ecological impact of ITS clade 6 associated with riparian ecosystems in plant disease on plant communities’, Journal of the South Africa and Australia’, Fungal Biology, Royal Society of Western Australia, vol. 77, vol. 117(5), pp. 329–347. pp. 127–131. Rea AJ, Jung T, Burgess TI, Stukely MJC & WWF & DCC 2004, ‘Arresting Phytophthora dieback: Hardy GEStJ 2010, ‘Phytophthora elongata sp. The biological bulldozer’, A report by the World nov., a novel pathogen from the Eucalyptus Wildlife Fund, (Gland, Switzerland) and the WA marginata forest of Western Australia’ Australasian Dieback Consultative Council, Western Australia, Plant Pathology, vol. 39(6), pp. 477–491. p. 22, . Rea AJ, Burgess TI, Hardy GEStJ, Stukely MJC & Jung T 2011, ‘Two novel and potentially endemic species of Phytophthora associated with episodic Information on other dieback of Kwongan vegetation in the south-west of Western Australia’, Plant Pathology, vol. 60(6), Phytophthora species pp. 1055–1068.

Aghighi S., Hardy GEStJ, Scott JK & Burgess TI 2012, Scott PM, Burgess TI, Barber PA, Shearer BL, ‘Phytophthora bilorbang sp. nov., a new species Stukely MJC, Hardy GEStJ & Jung T 2009, associated with the decline of ‘Phytophthora multivora sp. nov., a new species (European blackberry) in Western Australia’ recovered from declining Eucalyptus, Banksia, European Journal of Plant Pathology, vol. 133(4), and other plant species in Western pp. 841–855. Australia,’ Persoonia: Molecular Phylogeny and Evolution of Fungi . . Burgess TI, Webster JL, Ciampini JA, White D, , vol 22, pp 1–13. Hardy GEStJ & Stukely MJC 2009, ‘Re-evaluation of Phytophthora species isolated during 30 years of vegetation health surveys in Western Australia using molecular techniques’, Plant Disease, vol. 93(3), pp. 215–223.

33 Appendix C

State documents relevant to Phytophthora cinnamomi

State Document WESTERN AUSTRALIA Dieback working group publications (many of these documents have national applicability) Best practice guidelines: Management of Phytophthora dieback in extractive industries Managing Phytophthora dieback: Guidelines for local government Managing Phytophthora dieback in bushland: A guide for landholders and community conservation groups Flyers relating to phosphite use: • Phosphite injection using Chemjet Syringes • Dieback Treatment Spraying Native garden plants resistant to dieback (Phytophthora cinnamomi) Western Australian natives resistant to Phytophthora cinnamomi, compiled by Groves E, Hardy G & McComb J, Murdoch University Western Australian natives susceptible to Phytophthora cinnamomi, compiled by Groves E, Hardy G & McComb J, Murdoch University Phytophthora dieback management plan for the South Coast Region 2010–2017 (draft), . TASMANIA Keeping it clean - A Tasmanian field hygiene manual to prevent the spread of freshwater pests and pathogens.

This manual provides information on how to prevent the spread of freshwater pests and pathogens in Tasmanian waterways, wetlands, swamps and boggy areas. It is intended primarily for people who work in these areas, but also will help recreational visitors to understand the risks and act accordingly. Tasmanian Wilderness World Heritage Area Phytophthora cinnamomi Management Plan 2008–2017, unpublished, Tasmanian Parks and Wildlife Service. Conservation of Tasmanian plant species & communities threatened by Phytophthora cinnamomi: strategic regional plan for Tasmania, Technical Report 03/03, Schahinger R, Rudman T & Wardlaw TJ 2003, Nature Conservation Branch, Department of Primary Industries, Water and Environment, Hobart. Interim Phytophthora cinnamomi management guidelines, Nature Conservation Report 05/7, Rudman T (2005), Biodiversity Conservation Branch, Department of Primary Industries, Water and Environment, Hobart.

34 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi State Document QUEENSLAND Patch deaths in tropical Queensland rainforests: association and impact of Phytophthora cinnamomi and other soil borne organisms, Gadek PA (ed) 1999, Cooperative Research Centre for Tropical Rainforest Ecology and Management, Cairns, Queensland. Rainforest dieback: Risks associated with roads and walking track access in the Wet Tropics World Heritage Area, Worboys SJ & Gadek PA (2004), School of Tropical Biology, James Cook University Cairns Campus and Cooperative Research Centre for Tropical Rainforest Ecology and Management, Cairns, Queensland. Rainforest dieback mapping and assessment, 2004 monitoring report including an assessment of dieback in high altitude rainforests, Worboys SJ 2006, Cooperative Research Centre for Tropical Rainforest Ecology and Management, Cairns, Queensland. Guide to monitoring Phytophthora-related dieback in the Wet Tropics of North Queensland, Worboys SJ 2006, Cooperative Research Centre for Tropical Rainforest Ecology and Management. Rainforest CRC, Cairns, Queensland. VICTORIA Victoria’s public land Phytophthora cinnamomi management strategy, the State of Victoria, Department of Sustainability and Environment, 2008. NEW SOUTH WALES Infection of native plants by Phytophthora cinnamomi—key threatening process listing.

NSW Scientific Committee - final determination Statement of Intent 1: Infection of native plants by Phytophthora cinnamomi Department of Environment and Climate Change, NSW Best practice management guidelines for Phytophthora cinnamomi within the Sydney Metropolitan Catchment Management Authority Area. (2008). Facts about Phytophthora (brochure), Plant Disease Diagnostic Unit, Royal Botanic Gardens, Sydney. Phytophthora management in natural bushland—five strategies approach (brochure), Royal Botanic Gardens, Sydney SOUTH AUSTRALIA Phytophthora (dieback) control operational instruction 21.3, Transport SA - Statewide Operational Coordination Group 2000 Phytophthora management guidelines 2006, Phytophthora Technical Group, Government of South Australia.

35 Appendix D

Site variables that influence whether eradication or containment of Phytophthora cinnamomi is possible

Table prepared by the Western Australian Department of Environment and Conservation. Note: This assessment is based on Western Australian land systems and is not directly transferable to other land systems.

Eradication Level Eradication Level High probability of Medium probability success of success Containment Impact Reduction Size < 1 ha < 5 ha 5–500 ha Any size Soil type Deep sand Clay or rocky soils – – Vegetation condition High High–moderate High–moderate Low for high confidence occurrence mapping Level of infestation in Low Low Low Moderate–high surrounding native vegetation Hydrological Limited surface or Moderate surface Moderate surface Moderate – high characteristics of the subsurface runoff runoff and limited runoff and limited surface and site subsurface runoff subsurface runoff subsurface runoff Main mode of disease Root-to-root Mix of root-to-root Mix of root-to-root Movement in centre expansion and movement in and movement in surface and surface runoff surface run off subsurface run off Topography Flat Flat–moderate slopes Flat–moderate Moderate–steep slopes slopes Animal vectoring risk Low Low–moderate Low–moderate High Presence of declared No No No Yes rare flora or threatened ecological communities Presence of other No No Yes Yes values (e.g. aboriginal heritage sites, rare fauna) Proposed Methodology Vegetation Fencing, vegetation Fencing, root Phosphite treatment, destruction, destruction, herbicide impervious seed collection, herbicide treatment, treatment, phosphite membranes, translocation phosphite treatment, treatment, fumigation, phosphite treatment, fumigation root membranes, hydrological geo-textiles, engineering controls hydrological engineering controls Estimated cost per $50 000–$100 000 $100 000–$500 000 $20 000–$100 000 $1000–$100 000+ hectare

36 / Background: Threat abatement plan for disease in natural ecosystems caused by Phytophthora cinnamomi environment.gov.au BIO318.0114