Peter Scott

Estimates of invasion risk can support prioritisation of future threats from non-native species. Greater risk of invasion is expected when species occur in connected source regions and possess traits promoting successful transport, introduction or establishment. We compile a global database of first reports of Phytophthora de Bary species, a diverse oomycete genus attacking a broad range of plant hosts across multiple regions, sectors and ecosystem types with increasing frequency. Using Bayesian hierarchical zero-inflated models, we model global patterns of new detections since 2005 among 109 Phytophthora pathogens across 56 countries with at least two known Phytophthora species reported before 2005. We estimate the effects of trade connectivity, climate matching, national surveillance and pathogen traits on the probability of a new detection. We find that 69 (38%) Phytophthora species were either unknown or had no known source regions before 2005 and were therefore excluded from our analysis. Our study shows that invasion risk is increased for pathogens with broader thermal tolerance and the ability to produce survival structures linked to stress tolerance and asymptomatic infections. This knowledge can be used to enhance national horizon scanning and risk-based surveillance activities to better manage risks to plant health from emerging pathogens.

Phytophthora pathogens are responsible for causing disease in a range of environments, including natural, urban, nurseries and horticultural settings, and can be cryptically spread when present as inoculum in infected soil media. By evaluating the survival of Phytophthora inoculum in soil substrates without plants, their potential to be spread cryptically could be better understood. We tested the ability of Phytophthora multivora to survive in and be dispersed from sterile potting mix, forest soil and sand in the absence of plants when introduced as zoospores. We found that P. multivora zoospores readily encysted and survived in the potting mix for up to 76 days. The encysted zoospores were dispersed from the inoculated potting mix pots by overhead watering for up to 49 days. Zoospore cysts accumulated in the bottom sections of the potting mix pots as they were washed downward with each watering event. In contrast, P. multivora did not survive and persist in the sterile sand and forest soil substrates well. At 28 days-post-inoculation, only 10.1% of the destructively harvested replicates were positive with baiting for both sand and soil, while 100% of the potting mix reps were positive. The results raise concerns about the cryptic dispersal of inoculum during restoration projects especially from potting mix and show that zoospore cysts can contribute to the longer-term survival of Phytophthora inoculum. The potential presence of cryptic Phytophthora inoculum in nursery plants should be considered when sourcing plants for restoration projects to avoid inadvertently spreading soil-borne Phytophthora diseases.

The international spread of the myrtle rust pathogen, Austropuccinia psidii, can be largely attributed to the “pandemic” biotype that has more than 450 host species. However, within South America, the putative native range of A. psidii, multiple biotypes have been characterised, each with a restricted known number of hosts. These biotypes may pose a significant biosecurity threat to countries already affected by the pandemic biotype. Here, we report the susceptibility of four species of Myrtaceae from New Zealand, pōhutukawa (Metrosideros excelsa), mānuka (Leptospermum scoparium), kānuka (Kunzea ericoides), and rawiri mānuka (Kunzea ericoides ‘gumland ecotype’), to a strain of the Eucalyptus biotype of A. psidii. Symptoms and signs developed on inoculated plants of all species. Qualitative resistance phenotypes, with no disease development, were observed for all four species. However, no hypersensitive responses were observed. As seen for other biotypes, pōhutukawa had the greatest susceptibility, while kānuka had the lowest. These findings are consistent with prior work, showing that the Eucalyptus biotype can infect a broader range of species than its field host association implies. As well as uredinia (asexual spores), telia (sexual spores) developed on several plants, indicating that these species could provide a universal host for sexual reproduction and outcrossing between biotypes. Knowledge that the Eucalyptus biotype of A. psidii is virulent on several indigenous New Zealand Myrtaceae will inform future biosecurity risk assessments. These findings highlight the need to develop diagnostics tools to differentiate between biotypes and allow rapid responses to potential future incursions.

Phytophthora are causing declines in forest tree species worldwide and the chemical control treatment, phosphite, is the only treatment consistently shown to provide some protection to natural ecosystems from Phytophthora diseases. Phosphite inhibits Phytophthora growth and sporulation whilst boosting defence responses in the plant host. It is unclear, however, the extent of the impact of phosphite on Phytophthora species assemblages and inoculum abundances in soil around trees following treatment within natural ecosystems. In New Zealand, kauri (Agathis australis), an endemic and threatened foundation species, suffers from a dieback disease primarily caused by Phytophthora agathidicida. Phosphite is applied by trunk injection to kauri and has been shown to improve resin ‘bleed’ symptoms from basal trunk lesions and to promote recovery of thinned canopies. Phytophthora community and inoculum abundance were investigated in response to phosphite treatments at two field sites (Huia and Waitoki) in infected kauri stands in Auckland, New Zealand. At Huia, soil sampling and tree health surveying were conducted in November 2023 on trees treated with phosphite in 2012 as part of an earlier study. At Waitoki, the response to phosphite treatment was monitored 6 and 18 months following treatment. Phytophthora species were detected using soil baiting and metabarcoding of Environmental DNA (eDNA) from soil and quantified with qPCR of root and soil DNA. Three species were detected with soil baiting (P. agathidicida, P. cinnamomi, and P. multivora) and two additional species with metabarcoding (P. pseudocryptogea, and an unknown clade 7 species similar to P. europaea). Phytophthora cinnamomi was the most abundant species, followed by P. agathidicida. Both species were more likely to occur together than by chance alone and were associated with declining tree health. The P. europaea-like species was in approximately 50 % of the samples and was less likely to occur in roots with poorer health, or in association with P. agathidicida. The abundance of P. agathidicida inoculum was lower in the soil around the phosphite-treated trees than around the untreated control trees 1.5 years after treatment at Waitoki. Phosphite halted the lateral expansion of basal resin bleeds, and resin viscosity was reduced. Not only did phosphite treatments improve kauri dieback symptoms, but the phosphite treatments potentially had a direct impact on the epidemiology of the disease by reducing inoculum load around treated trees, with direct implications for disease management as an effective way to protect uninfected areas and minimise the spread of inoculum from infested zones.

Studies of Phytophthora impact in forests generally focus on individual species without recognition that Phytophthora occur in multispecies communities. This study investigated community structure of Phytophthora species in the rhizosphere of Agathis australis (kauri) in Te Wao Nui o Tiriwa/Waitākere Ranges, New Zealand, in the context of kauri dieback disease expression. Soil sampling and tree monitoring were conducted on 767 randomly selected mature kauri trees. Phytophthora species were detected using both soil baiting and DNA metabarcoding of environmental DNA (eDNA). Four species were detected with soil baiting (P. agathidicida, P. cinnamomi, P. multivora, and P. pseudocryptogea/P. cryptogea) and an additional three species with metabarcoding (P. kernoviae, P. cactorum/P. aleatoria and an unknown clade 7 species). Phytophthora cinnamomi was the most abundant species and was distributed throughout the forest. Both P. multivora and P. agathidicida were limited to forest edges, suggesting more recent introductions. P. agathidicida presence was strongly correlated with declining canopy health, confirming its role as the main driver of kauri dieback. The limited distribution of P. agathidicida and infrequent detections (11.0% samples) suggests that that this species is spreading as an introduced invasive pathogen and provide hope that with strategic management (including track upgrades and closures, restricting access to uninfected areas, and continual monitoring) uninfected areas of the forest can be protected. The frequent detections of P. cinnamomi and P. multivora from symptomatic trees in the absence of P. agathidicida suggest more research is needed to understand their roles in kauri forest health.

Context
Forest ecosystems experience compositional and structural changes as species’ environmental envelopes shift with climate change. Extreme climate events and pests/pathogens are driving these ecosystem changes. Determining which of the two potential drivers is causing a particular forest die-off can be challenging. In south-western Australia, widespread forest die-off in 2011 coincided with extremely hot and dry conditions. It occurred in a forest ecosystem that has historically experienced Phytophthora cinnamomi root disease (Phytophthora dieback).

Aims
To determine whether the causal agent of Phytophthora dieback, P. cinnamomi, was associated with forest die-off in the Northern Jarrah Forest.

Methods
A combination of direct (isolation of pathogen) and indirect (survey of susceptible indicator plant species) measurements were taken inside and outside patches of forest experiencing the die-off.

Key results
There was no consistent association between die-off patches and the presence of P. cinnamomi. P. cinnamomi was isolated from 3 of 33 control plots and 3 of 33 die-off plots. Although several plant species susceptible to P. cinnamomi were absent from die-off plots, the findings were inconsistent across species. This may be explained by plant tolerance to high temperatures and drought.

Conclusions
P. cinnamomi was not the proximate cause of the observed die-off in the Northern Jarrah Forest in 2011.

Implications
Novel disturbance caused by extreme climate events can mimic damage caused by certain pests/pathogens. More research is needed to determine the tolerances of plants to extreme temperature and drought conditions to disentangle abiotic and biotic drivers of tree die-off.

Global concerns are many for the invasive impacts of Phytophthora pathogens on native vegetation, agriculture, nurseries, and urban parks and gardens. We compiled a database of 32 traits on 204 species of Phytophthora including data on each species' taxonomy (clade and subclade), historical knowledge (years since first described), impacted ecosystems, microenvironments inhabited, dispersal mode, physiology, and morphology. Drawing from approximately 11,394 unique host, pathogen, and country plant disease records from GenBank and other sources, we calculated potential invasiveness of 103 better studied species from cluster relationships. We used the species data to create a Bayesian network model predicting the degree and probability of invasiveness of individual Phytophthora species. Model calibration testing resulted in <1% error rate in classifying invasiveness categories of well‐known species. We applied the model to predict the potential invasiveness of 101 other species with unknown invasiveness dynamics. The model can also be used to predict the invasive risk of other poorly studied and newly identified Phytophthora species, and the general modeling approach can be used for other pests and pathogens, to advise land and resource managers to thwart potential invasions before they occur or intensify.

Among the most economically relevant and environmentally devastating diseases globally are those caused by Phytophthora species. In Australia, production losses in agriculture and forestry results from several well-known cosmopolitan Phytophthora species and infestation of natural ecosystems by Phytophthora cinnamomi have caused irretrievable loss to biodiversity, especially in proteaceous dominated heathlands. For this review, all available records of Phytophthora in Australia were collated and curated, resulting in a database of 7869 records, of which 2957 have associated molecular data. Australian databases hold records for 99 species, of which 20 are undescribed. Eight species have no records linked to molecular data, and their presence in Australia is considered doubtful. The 99 species reside in 10 of the 12 clades recognised within the complete phylogeny of Phytophthora. The review includes discussion on each of these species? status and additional information provided for another 29 species of concern. The first species reported in Australia in 1900 was Phytophthora infestans. By 2000, 27 species were known, predominantly from agriculture. The significant increase in species reported in the subsequent 20 years has coincided with extensive surveys in natural ecosystems coupled with molecular taxonomy and the recognition of numerous new phylogenetically distinct but morphologically similar species. Routine and targeted surveys within Australian natural ecosystems have resulted in the description of 27 species since 2009. Due to the new species descriptions over the last 20 years, many older records have been reclassified based on molecular identification. The distribution of records is skewed toward regions with considerable activity in high productivity agriculture, horticulture and forestry, and native vegetation at risk from P. cinnamomi. Native and exotic hosts of different Phytophthora species are found throughout the phylogeny; however, species from clades 1, 7 and 8 are more likely to be associated with exotic hosts. One of the most difficult challenges to overcome when establishing a pest status is a lack of reliable data on the current state of a species in any given country or location. The database compiled here for Australia and the information provided for each species overcomes this challenge. This review will aid federal and state governments in risk assessments and trade negotiations by providing a comprehensive resource on the current status of Phytophthora species in Australia.

Phytophthora agathidicida is the accepted causal agent of dieback in remnant stands of long-lived indigenous New Zealand kauri (Agathis australis) and poses a significant threat to the long-term survival of this species. Little is known about the effect of key soil physicochemical characteristics on the growth of P.agathidicida. In this study, we investigated the growth of P.agathidicida in soils collected from adjacent areas under original kauri forest, short rotation pine (Pinus radiata) plantation forest and grazed pastures. A growth response assay was used to quantify asexual (sporangia) and sexual (oospore) spore counts over 8days in soils sampled from each land-use. Significantly higher numbers of sporangia (p<0.001) and oospores (p<0.01) were found in pasture and pine forest soil within 2days of the growth assay trials, suggesting these soils may favour asexual/sexual reproduction in the early stages of P.agathidicida establishment compared to kauri forest soils. Additionally, oospore production significantly increased over 8days in pine forest soil, suggesting that with an increase in inoculum loads, these soils potentially act as pathogen reservoirs. The soil physicochemical properties (e.g., pH, C and N, phosphorus content and electrical conductivity) investigated in this study did not significantly correspond to spore count data between land-uses, suggesting that differences in growth response are driven by other edaphic factors not explored in the present study.

This article provides a brief overview of the status of Phytophthora diseases in New Zealand forests. Recent outbreaks of Phytophthora diseases internationally and within these forests, including Red Needle Cast of Pinus radiata caused by Phytophthora pluvialis and Agathis australis (kauri) dieback caused by Phytophthora taxon Agathis (PTA), have highlighted the biosecurity threat these species pose to New Zealand. In isolated cases, Red Needle Cast has impacted P. radiata plantations through the premature defoliation of mature needles. Kauri dieback, caused by Phytophthora taxon Agathis, has resulted in devastating disease within some sites. Preliminary research indicates that both these diseases will respond to treatment with phosphite, consistent with current international Phytophthora management. Ongoing research into Red Needle Cast, Phytophthora taxon Agathis induced kauri dieback and other Phytophthora diseases within P. radiata and kauri is focusing on understanding the epidemiology of the diseases, the chemical and genetic mechanisms of resistance, and also screening for durable resistance to multiple Phytophthora species. Many other Phytophthora pathogens have been identified within New Zealand. These have not been found to cause serious disease in native or exotic forest systems, despite some being known to cause diseases of great consequence internationally. Significant examples include P. cinnamomi, P. multivora and P. kemoviae. As a result of increased global movement of plant material, New Zealand's and other international forests are vulnerable to new Phytophthora diseases. However, through the world's best practice adaptive management the threat and impacts of these diseases can be reduced.