Quantifying the Distribution and Threat of Phytophthora Cinnamomi in New South Wales: Implications for Its Management in Natural Vegetation
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Cunninghamia Date of Publication: August 2020 A journal of plant ecology for eastern Australia ISSN 0727- 9620 (print) • ISSN 2200 - 405X (Online) Quantifying the distribution and threat of Phytophthora cinnamomi in New South Wales: implications for its management in natural vegetation Keith L McDougall1 & Edward CY Liew2 1Department of Planning, Industry and Environment, PO Box 733, Queanbeyan NSW 2620 AUSTRALIA 2 Australian Institute of Botanical Science, The Royal Botanic Gardens and Domain Trust, Mrs Macquaries Road, Sydney NSW 2000 AUSTRALIA Abstract: Phytophthora cinnamomi is an oomycete (water mould) with a large host range. It infects plants through their roots and in some cases will kill them. The pathogen is readily dispersed in soil and water, over short distances by its swimming spores and over large distances by humans. While Phytophthora cinnamomi has been well-studied in other parts of Australia, its distribution and impact are poorly known in New South Wales (NSW). In the current study we compiled existing data on Phytophthora cinnamomi occurrence and filled spatial gaps in sampling. We found about 1000 records of Phytophthora cinnamomi presence in over 5000 tests of soil and root material, and collected a further 457 samples from areas where no sampling had previously been done. The resulting data set enabled modelling of Phytophthora cinnamomi habitat suitability using the software program MaxEnt with climate and soil spatial layers. We found that coastal areas and adjacent tablelands were most suitable for the pathogen, although some areas within that may be unsuitable because of soil properties. We then modelled assets (threatened species) potentially affected by Phytophthora cinnamomi to produce a layer of risk. Using projected climate layers, we found that habitat suitability and risk will decline in parts of northern NSW by 2070 but be amplified in the south. New susceptible species in places such as the Australian Alps are likely to be exposed to the pathogen in the future. We offer advice for managing Phytophthora cinnamomi in NSW. Management is difficult where the effects of this pathogen are often inconspicuous and its distribution is widespread. However, basic hygiene to limit spread to susceptible assets will have great benefit regardless. Cunninghamia (2020) 20: 153–181 doi: 10.7751/cunninghamia.2020.20.008 Cunninghamia: a journal of plant ecology for eastern Australia © 2020 Royal Botanic Gardens and Domain Trust www.rbgsyd.nsw.gov.au/science/Scientific_publications/cunninghamia 154 Cunninghamia 20: 2020 McDougall & Liew, Phytophthora cinnamomi in NSW Introduction of these, the chlamydospore, is relatively long-lived and durable, enabling the pathogen to survive prolonged dry Phytophthora cinnamomi is an oomycete (water mould), periods (Jung et al. 2013a). Chlamydospores can germinate which is thought to have originated in south-east Asia to produce mycelia and sporangia and ultimately, more (Dobrowolski et al. 2003), although there is evidence for one zoospores (McCarren et al. 2005). The sexual part of the strain having an Australasian origin (Arentz 2017). It can life cycle leading to the production of oospores requires now be found in all continents (except Antarctica) where it the presence of the two mating types, A1 and A2. The A1 has a range of economic and environmental impacts (Cahill strain is rare in Australia (e.g. Weste and Marks 1987) and et al. 2008). Hosts of economic importance include avocado, sexual reproduction, if it occurs, is also rare. Phytophthora chestnut, grapes, pineapple and commercial forestry species cinnamomi is effectively asexual in Australia. (Cahill et al. 2008). The pathogen can also have catastrophic Phytophthora cinnamomi spreads in soil and water but, effects in native vegetation (e.g. in oak forests of Europe importantly, is not airborne. It may spread over short (Jung et al. 2013b) and heathlands in South Africa (Von distances from one root to another by motile zoospores or by Broembsen & Kruger 1985)) but has had the most dramatic the growth of mycelium on closely contacting roots (i.e. cm effect in southern Western Australia (Shearer et al. 2007). to a few metres; e.g. Hill et al. 1994). However, the pathogen As a consequence, it is regarded as one of the 100 world’s may move longer distances within a site in run-off after worst invasive alien species in the Global Invasive Species storm events (i.e. 100s of metres; Kinal et al. 1993) or when Database (Lowe et al. 2000), and has been listed as a key moved by animals in infested soil (i.e. many km; Cahill et al. threat to biodiversity in several Australian jurisdictions. 2008). Soil may be spread by non-human animals on hooves and even in faeces (Li et al. 2014) but this will typically be on the scale of home ranges (usually a few to several km2). Humans, however, tend to spread it furthest because they can travel much longer distances than non-human animals (e.g. in cars, with heavy machinery, on bikes and horses, or when bushwalking). The relative importance of different dispersal vectors has not been quantified but humans are likely to be the most significant dispersal agents for conservation management because they can rapidly spread it over vast distances and across natural dispersal barriers (e.g. mountain ranges). In the absence of hygiene measures, the likelihood and magnitude of spread by dispersal vectors can be thought of in terms of the quantity of soil that can be dispersed, the distance it can be dispersed and the frequency of dispersal (e.g. a bulldozer carries greater risk of spread than a kangaroo or goat). Once Phytophthora cinnamomi is introduced to a new area it is practically impossible to eradicate (Dunstan et al. 2010). The host range of Phytophthora cinnamomi is huge globally (Zentmyer 1980) and in Australia (O’Gara et al. 2006). Some species will be unaffected in the presence of the pathogen or asymptomatic (Phillips & Weste 1984; Crone et al. 2013), Fig. 1. Life cycle of Phytophthora cinnamomi. Reproduced with while others are highly susceptible under most conditions. permission from Hardham (2005). Several common Australian plant families have large numbers of susceptible hosts (e.g. Ericaceae, Proteaceae). Loss of Phytophthora cinnamomi colonises plants through roots or dominant species to infection by Phytophthora cinnamomi plant collars. It is a necrotroph, feeding on live cells and often may result in major vegetation change with adverse effects killing plant hosts, rather than a saprophyte, which feeds on on other elements of ecosystems. Several animal species, plant material that is already dead. Its life cycle involves for instance, are indirectly at risk because of habitat change a range of stages and spore types (Hardham 2018; Fig. 1). and loss of food plants (e.g. the honey possum, Dundas In its vegetative stage, mycelial strands spread in its host, et al. 2016). Diverse heathy woodlands in Victoria have been damaging the plant’s water and nutrient conducting tissues. transformed into communities dominated by tolerant grasses For that reason, plant death often mimics the effects of severe and sedges (e.g. Weste et al. 2002). Some species are being drought. Mycelial strands may also spread from host to host pushed towards extinction because of this pathogen. In the through contact between roots. Under moist conditions, current threat abatement plan for Phytophthora cinnamomi, short-lived motile zoospores are produced from sporangia on 121 threatened plant taxa are reported to be susceptible to the mycelia, which enable dispersal to nearby hosts. Other infection (Department of Environment and Energy 2018). spore types may be produced under certain conditions. One Cunninghamia 20: 2020 McDougall & Liew, Phytophthora cinnamomi in NSW 155 The expression of disease requires three elements: presence vegetation in WA. The origin of such Phytophthora species of the pathogen, presence of a host and suitable conditions for could be investigated genetically but, without adequate colonisation and disease development. Suitable conditions resources, most will remain as being of uncertain origin. are not simply a function of the average (prevailing) climate With climate and land use change, and the likely movement at any site. Stress is likely to play a major role in disease of native and non-native pathogens to new areas, the origin expression. Climate extremes (e.g. drought, flooding) and the of these species is perhaps irrelevant. If they are affecting co-occurrence of other pathogens and insect pests may place ecosystems in a unidirectional way, their effects are worth normally tolerant species at risk. This will become especially taking seriously. At least the A2 strain of Phytophthora important as climate changes. Substantial variation in the cinnamomi is likely to be non-native in New South Wales; pathogenicity of isolates of Phytopthora cinnamomi has also this strain is the more common and is responsible for most been reported (Dudzinski et al. 1993) and so it is possible damage. In the current paper we have little regard for the that the pathogen may have differing impacts across the origin of Phytophthora cinnamomi but focus on its impacts range of a single vegetation type or susceptible species. and the consequent needs of conservation management. In Predicting disease where disease expression is stochastic addition, the future distribution of Phytophthora cinnamomi and pathogenicity is variable can therefore be extremely is likely to change as climate changes, and its climate related challenging, making management problematic. In addition, movement will occur more quickly than that of its hosts. some areas where disease is predicted based on climate and New vascular plant species are likely to be affected while the presence of hosts may not be affected because of soil others may be released from its effects. Greater stress on properties. For instance, Phytophthora cinnamomi is known plants from extreme and changing conditions could also to have poor survival and minimal impact in highly organic make some species vulnerable where they were apparently soils (Halsall 1982) and those with high levels of calcium tolerant in the past.