Phytophthora ramorum (sudden oak death (SOD))
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PicturesTop of page
|Title||Stem canker |
|Caption||Aerial stem canker caused by P. ramorum on a tan oak.|
|Copyright||Matteo Garbelotto/U.C. Berkeley, USA|
|Stem canker ||Aerial stem canker caused by P. ramorum on a tan oak.||Matteo Garbelotto/U.C. Berkeley, USA|
|Caption||Bark seeping on a coast live oak infected by P. ramorum.|
|Copyright||Matteo Garbelotto/U.C. Berkeley, USA|
|Bark seeping||Bark seeping on a coast live oak infected by P. ramorum.||Matteo Garbelotto/U.C. Berkeley, USA|
|Caption||Lesions on leaves of Umbellularia californica caused by P. ramorum.|
|Copyright||Matteo Garbelotto/U.C. Berkeley, USA|
|Leaf lesions||Lesions on leaves of Umbellularia californica caused by P. ramorum.||Matteo Garbelotto/U.C. Berkeley, USA|
|Caption||Sporangia of P. ramorum releasing zoospores.|
|Copyright||David Rizzo/U.C. Davis, USA|
|Sporangia||Sporangia of P. ramorum releasing zoospores.||David Rizzo/U.C. Davis, USA|
|Caption||Chlamydospores of P. ramorum.|
|Copyright||David Rizzo/U.C. Davis, USA|
|Chlamydospores||Chlamydospores of P. ramorum.||David Rizzo/U.C. Davis, USA|
IdentityTop of page
Preferred Scientific Name
- Phytophthora ramorum Werres, De Cock & Man in't Veld
Preferred Common Name
International Common Names
- English: ramorum blight
- Spanish: muerte repentina de los robles
- PHYTRA (Phytophthora ramorum)
Summary of InvasivenessTop of page
Phytophthora ramorum is considered an invasive species due to its ability to spread, persist, and reproduce in new environments. Its rapid life-cycle, propensity to reproduce asexually and spread aerially (via windblown rain), plus its ability to survive through harsh climatic conditions, are elements favouring this species’ potential invasiveness. Its broad host range on popular, nursery grown, ornamental plants, and the non-lethal, nondescript nature of the disease on most of the foliar hosts allows for long-term dispersal. Genetic analysis shows P. ramorum infection occurs only in Europe and parts of North America; three clonal lineages have been identified: EU1, NA1 and NA2. Information to date indicates that divergence of these lineages occurred ages ago, P. ramorum originated from isolated populations and has migrated at least four times to North America and Europe (Grunwald et al., 2011).
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Chromista
- Phylum: Oomycota
- Class: Oomycetes
- Order: Peronosporales
- Family: Peronosporaceae
- Genus: Phytophthora
- Species: Phytophthora ramorum
Notes on Taxonomy and NomenclatureTop of page
On the basis of DNA data and morphological traits such as sporangia and chlamydospores, P. ramorum belongs to clade 8c, closely related to Phytophthora lateralis, a pathogen of Chamaecyparis lawsoniana (Port Orford cedar) and Phytophthora hibernalis, a pathogen of many orchard tree species. This clade is more distantly related to a group of species including Phytophthora syringae, P. cryptogea, P. trifolii and P. drechsleri, among others. Draft whole-genome (Tyler et al., 2006) and mitochondrial (Martin et al., 2007) sequences of P. ramorum are available.
DescriptionTop of page
Sporangia are hyaline, ellipsoid or elongated-ovoid (length x width = 25-97 x 14-34 µm, mean 46-65 x 21-28 µm), sympodial, semipapillate, and deciduous, carried on a short stalk. They are produced readily on most media if plant material is included. They are also produced on V8 agar plates, although not consistently. Chlamydospores are large, round, hyaline or yellow-cinnamon depending on substrate. They can be terminal and intercalary or more rarely lateral, and are a good diagnostic feature, especially because of their size (20-91 µm, mean 46-60 µm). P. ramorum is a heterothallic, amphigynous species, and both mating types are known in nature but do not readily form sexual spores when artificially crossed. Measurements of mature gametangia are as follows: oogonial diameter, mean 30.5 µm, range 25-35 µm; oospore diameter, mean 25.5 µm, range 22.5-27.5 µm; antheridial width, mean 17.3 µm; antheridial length, mean 15.0 µm. Growth is optimal at 18-20°C: a relatively slow grower. Hyphae are often extremely knobbly, although they lack swellings, and abundant septation can be observed, especially when producing chlamydospores. Mycelium is appressed, forming concentric growth rings more or less pronounced based on the type of media (Werres et al., 2001).
DistributionTop of page
In Europe, P. ramorum has been reported in commercial nurseries in over 20 countries, and is under regulatory control (Sansford et al., 2009). Outside of nurseries, infection appears limited to ornamental plants in gardens and scattered woodland trees and shrubs until 2009, when extensive mortality and infection erupted in the UK, on Japanese larch (Larix kaempferi) in timber plantations (Brasier and Webber, 2010).
In North America, the pathogen has been detected in over 400 ornamental nurseries where it is under regulatory control requiring eradication (Frankel and Hansen, 2011). In wildlands the disease is patchy but widespread along the central coast of California and south-west Oregon. In Oregon, P. ramorum has been identified on over 500 sites in Curry County. An eradication effort was conducted from 2001 to 2011, but in 2012 regulations were revised to promote containment.
In California, the pathogen is widespread but only in central coastal regions. It is absent in all other regions, including the southern coastal area and the mountain ranges of the interior. In the infested area, distribution is extremely patchy and variable (Kelly and Meentemeyer, 2002; Swiecki and Bernhardt, 2002; Meentemeyer et al., 2011). Estimates of infection rates and number of trees killed by the disease are extremely difficult since they are so numerous. The following counties are infested: Humboldt, Mendocino, Napa, Lake, Sonoma, Solano, Contra Costa, Alameda, Marin, San Mateo, Santa Clara, Santa Cruz, San Francisco and Monterey. The disease appears to have doubled coast live oak (Quercus agrifolia) mortality rates and quadrupled tanoak (Notholithocarpus densiflorus, formerly known as Lithocarpus densiflorus) mortality rates (McPherson et al., 2002; Swiecki and Bernhardt, 2002). Mortality rates are greater than 50% in some areas and continue to increase (Maloney et al., 2005; Swiecki and Bernhardt, 2008).
P. ramorum has also been detected in waterways adjacent to infested nurseries in Florida, Mississippi, Alabama, Georgia and other states (Chastagner et al., 2009).
Despite extensive surveys for P. ramorum across Canada, it has only been found in nurseries in British Columbia and is under active eradication (IPPC, 2009).
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Country||Distribution||Last Reported||Origin||First Reported||Invasive||References||Notes|
|India||Restricted distribution||CABI/EPPO, 2013|
|-Kerala||Restricted distribution||CABI/EPPO, 2013|
|Canada||Present, few occurrences||CABI/EPPO, 2013; IPPC, 2009; EPPO, 2014|
|-British Columbia||Present, few occurrences||CABI/EPPO, 2013; EPPO, 2014|
|USA||Restricted distribution||EPPO, 2014; CABI/EPPO, 2013|
|-California||Restricted distribution||Rizzo et al., 2002a; EPPO, 2011; EPPO, 2014; Blomquist et al., 2012; CABI/EPPO, 2013; Garbelotto et al., 2014|
|-Florida||Present, few occurrences||EPPO, 2014; CABI/EPPO, 2013|
|-Georgia||Present, few occurrences||EPPO, 2014; CABI/EPPO, 2013|
|-Louisiana||Present, few occurrences||EPPO, 2014; CABI/EPPO, 2013|
|-North Carolina||Absent, confirmed by survey||EPPO, 2014|
|-Oklahoma||Absent, confirmed by survey||EPPO, 2014|
|-Oregon||Restricted distribution||Goheen et al., 2002a; EPPO, 2014; CABI/EPPO, 2013; Grünwald et al., 2016|
|-South Carolina||Present, few occurrences||EPPO, 2014; CABI/EPPO, 2013|
|-Tennessee||Present, few occurrences||EPPO, 2014; CABI/EPPO, 2013|
|-Texas||Absent, confirmed by survey||EPPO, 2014|
|-Virginia||Present||EPPO, 2014; CABI/EPPO, 2013|
|-Washington||Present||CABI/EPPO, 2013; EPPO, 2014|
|Austria||Absent, confirmed by survey||EPPO, 2014|
|Belgium||Restricted distribution||Werres et al., 2001; EPPO, 2014; CABI/EPPO, 2013|
|Croatia||Restricted distribution||EPPO, 2014; EPPO, 2011; CABI/EPPO, 2013|
|Czech Republic||Transient: actionable, under eradication||EPPO, 2014; EPPO, 2011; CABI/EPPO, 2013|
|Denmark||Present, few occurrences||EPPO, 2014; CABI/EPPO, 2013|
|Estonia||Absent, confirmed by survey||EPPO, 2014|
|Finland||Transient: actionable, under eradication||EPPO, 2014; CABI/EPPO, 2013|
|France||Transient: actionable, under eradication||EPPO, 2014; CABI/EPPO, 2013|
|Germany||Restricted distribution||Werres & Marwitz, 1997; EPPO, 2014; CABI/EPPO, 2013|
|Greece||Present, few occurrences||EPPO, 2014; Tsopelas et al., 2011; CABI/EPPO, 2013|
|Ireland||Restricted distribution||EPPO, 2011; EPPO, 2014; CABI/EPPO, 2013|
|Italy||Transient: actionable, under eradication||EPPO, 2014; CABI/EPPO, 2013; Ginetti et al., 2014|
|Latvia||Absent, intercepted only||EPPO, 2014|
|Lithuania||Absent, confirmed by survey||EPPO, 2014; CABI/EPPO, 2013; IPPC, 2016|
|Netherlands||Restricted distribution||EPPO, 2014; IPPC, 2006; CABI/EPPO, 2013; NPPO of the Netherlands, 2013|
|Norway||Present||Rytkönen et al., 2012; EPPO, 2014; CABI/EPPO, 2013|
|Poland||Present, few occurrences||Orlikowski & Szkuta, 2002; EPPO, 2014; CABI/EPPO, 2013|
|Portugal||Absent, confirmed by survey||EPPO, 2014; Gomes & Amaro, 2008; CABI/EPPO, 2013|
|Serbia||Present, few occurrences||EPPO, 2014; Bulajic et al., 2010; CABI/EPPO, 2013|
|Slovakia||Absent, confirmed by survey||EPPO, 2014|
|Slovenia||Present, few occurrences||EPPO, 2014; CABI/EPPO, 2013|
|Spain||Present, few occurrences||Moralejo & Werres, 2002; EPPO, 2014; CABI/EPPO, 2013|
|-Balearic Islands||Present||EPPO, 2014; CABI/EPPO, 2013|
|-Spain (mainland)||Present||CABI/EPPO, 2013|
|Sweden||Restricted distribution||EPPO, 2014; CABI/EPPO, 2013|
|Switzerland||Present, few occurrences||EPPO, 2014; CABI/EPPO, 2013|
|UK||Restricted distribution||Brasier & Webber, 2012; EPPO, 2014; CABI/EPPO, 2013; King et al., 2015|
|-Channel Islands||Present, few occurrences||EPPO, 2014; CABI/EPPO, 2013|
|-England and Wales||Restricted distribution||Giltrap et al., 2004; EPPO, 2014; CABI/EPPO, 2013|
|-Scotland||Restricted distribution||EPPO, 2014; CABI/EPPO, 2013|
Risk of IntroductionTop of page
P. ramorum is a quarantined pest in California and southern Oregon, USA (other than nurseries, the rest of Oregon is not quarantined due to wildland eradication and containment efforts). All host plants are regulated in nurseries shipping out of state in Washington, Oregon and California.
The USA, the EU, Canada, New Zealand, Australia, the Czech Republic, Mexico, Taiwan, South Korea and other countries have identified P. ramorum as a quarantine pest (Frankel, 2008). The European Union Pest Risk Analysis for P. ramorum (Sansford et al., 2009) lists 68 countries that mention P. ramorum in their regulations (Kliejunas, 2010).
HabitatTop of page
Natural habitats include a few types of coastal California forests. The first is the mixed evergreen forest characterized by coast live oak (Quercus agrifolia), California bay laurel (Umbellularia californica) and Pacific madrone (Arbutus menziesii). The second is the tanoak-redwood forest, characterized by redwood (Sequoia sempervirens) dominance, with a significant tanoak (Notholithocarpus densiflorus), California bay laurel and Douglas fir (Pseudotsuga menziesii) component (Rizzo et al., 2002a, b; Garbelotto et al., 2003). In 2009, the pathogen was found infecting tanoak in a bishop pine (Pinus muricata) forest along the Mendocino Coast (Frankel and Hansen, 2011). In Oregon impacted forests are dominated by tanoak and Douglas fir with red alder (Alnus rubra) and Oregon myrtlewood (California bay laurel) (Umbellularia californica) (Hansen et al., 2008).
Hosts/Species AffectedTop of page
Quercus rubra, Q. palustris, Pittosporum undulatum and many other species are regarded as potential hosts: for these species, inoculation experiments have been completed, confirming susceptibility, but no natural infection has been recorded to date (2003). A database of species tested for susceptibility is available at the Risk Analysis for Phytophthora ramorum website (http://rapra.csl.gov.uk/). More information on host range is given in the following references: Werres et al. (2001); Davidson et al. (2002a); Hansen and Sutton (2002); Linderman et al. (2002); Maloney et al. (2002); Parke et al. (2002); Rizzo et al. (2002a, b); Tooley and Englander (2002); Garbelotto et al. (2003); Huberli et al. (2003) and Kliejunas (2010). A host list is maintained by the USDA Animal and Plant Health Inspection Service (http://www.aphis.usda.gov/plant_health/plant_pest_info/pram/downloads/pdf_files/usdaprlist.pdf). To date (2012) there are over 120 species listed. The California Oak Mortality Task Force (www.suddenoakdeath.org) also maintains a host list with photos of symptoms.
In 2009, P. ramorum was confirmed as the cause of extensive dieback and mortality in mature and juvenile Japanese larch (Larix kaempferi) at a number of sites in south-west England. In 2010, P. ramorum was isolated from larch plantations displaying similar symptoms in south Wales. Overall, 2400 ha or ca. 0.6 million mature larch were affected (Webber et al., 2011) in addition to a large area of juvenile larch. This is the first widespread and lethal damage caused by P. ramorum to a commercially important conifer species anywhere in the world. Secondary infection of Fagus sylvatica, Nothofagus obliqua, Castanea sativa, Betula pendula, Rhododendron ponticum, Tsuga heterophylla and Pseudotsuga menziesii was found adjacent to some affected larch sites in south-west England.
Yaupon (Ilex vomitoria), sweetbay magnolia (Magnolia virginiana) and baldcypress (Taxodium distichum) were reported as hosts of P. ramorum when several plant species native to the Gulf Coast and south-eastern US forests were tested for reaction to P. ramorum (Preuett et al., 2013).
Growth StagesTop of page
Flowering stage, Fruiting stage, Post-harvest, Seedling stage, Vegetative growing stage
SymptomsTop of page
P. ramorum causes three distinct types of disease with corresponding symptoms.
Stem Cankers (Rizzo et al., 2002a).
The cankers resemble those caused by other Phytophthora species. Discoloration can be seen in the inner bark, the cambium and within the first few sapwood rings. Discoloration is always associated with the cankers, but its intensity is extremely variable, ranging from dark-brown, almost black, lesions to slight discoloration of the infected tree tissue. Black zone lines are often, but not always, present at the edge of the cankers. Smaller tanoaks (Notholithocarpus densiflorus) tend not to have any zone lines. Most notably, P. ramorum cankers stop abruptly at the soil line, and there are few reports of root infection in tanoak. Viburnum is the only host in which root collar infection is common (Werres et al., 2001). Typical bleeding symptoms can be seen on the outside of the cankers. Bleeding is not necessarily associated with cracks or wounds, and tends to be rather viscous in consistency. A distinct fermentation smell (or alcoholic smell) emanates from bark seeps. Intensity and viscosity of bleeding changes with time. Older cankers may display a thin, brown-amber crust where seeps were originally present. Crown symptoms are often associated with expansion rate of cankers. Rapidly expanding cankers rapidly girdle the tree. In this case, there is no real crown decline, but once the tree has exhausted the resources accumulated in its aerial part, the whole crown browns. The entire foliage turns orange-brown and then becomes grey with time. The name 'sudden oak death' was coined because of the high frequency of rapidly declining trees. In the phase between girdling and apparent death of the crown, secondary processes are initiated. These include growth and fruiting of Annulohypoxylon thouarsianum, syn. Hypoxylon thouarsianum. A. thouarsianum will cause a mottled decay of portions of the sapwood and will fruit abundantly on the bark. Other secondary processes include attacks by bark and ambrosia beetles and acceleration of decay processes, at times with basidiocarps produced on trees which are still green.
When cankers are slow-growing, typical decline symptoms can be seen in the crown and include: chlorosis of the foliage, premature leaf abscission resulting in sparse crowns, and sometimes dieback of branches corresponding to portions of the stem affected by the canker. Epicormic shoots are often associated with both types of cankers (slow and fast). On oak species, most cankers are found within 1 m of the root collar, but cankers higher up on the stem and on major branches are not uncommon. Oak leaves, twigs, and juvenile plants are rarely infected. Tanoak cankers tend to be present throughout the vertical length of the tree and most trees have multiple cankers on them. Plants of all ages can be infected and killed. Leaves and twigs can also be infected. Foliar infection can precede or follow twig infection and it results in leaf spotting and a characteristic blackening of the main rib of the leaf, with lesions continuing into the petiole.
Leaf Blight and Branch Dieback (Rizzo et al., 2002b; Garbelotto et al., 2003).
Leaves develop lesions often associated with twig dieback. The primary infection court can be either in the twig or in the leaf. Cankers develop on branches. Symptoms on leaves develop rather rapidly and may result in death of the leaf. Rhododendron spp., Pieris spp. and Rhamnus spp. display these symptoms. In ericaceous hosts with small leaves (e.g. Vaccinium ovatum and Arctostaphylos spp.), foliar symptoms are not as pronounced. Leaf abscission and cane cankers are more common, resulting in the death of clumps of branches. Symptoms on coniferous hosts such as Douglas fir (Pseudotsuga menziesii) and Grand fir (Abies grandis) fall into this general category. In these two hosts, branch tips are typically affected. Branch tips, especially the last year's growth, are girdled and will wilt. Needles hang from the infected branch at first and then will drop, leaving a barren branch tip appearing similar to browse injury.
Leaf Spots, Blotches, and Scorches (Rizzo et al., 2002b; Garbelotto et al., 2003).
In some hosts, the disease affects leaves but not the twigs or branches. Lesions are normally associated with the accumulation of water on the leaf. These symptoms are in general rather nondescript. Lesions on Umbellularia californica are generally dark in colour, often at the leaf tip where water accumulates. Lesions are generally demarcated by an irregular margin, often followed by a chlorotic halo. Premature chlorosis of the entire leaf, followed by its abscission, is common in drier areas. Infection in Aesculus californica starts as light circular spots, coalescing into large blotches often affecting the whole leaf, and at times the petiole. In Acer macrophyllum, symptoms appear as a marginal leaf scorch. The scorch does not, at least initially, affect the whole leaf contour, and scorched portions are interrupted by healthy areas.
On redwood the disease affects mostly needles of the lower branches. Needles appear to be infected individually, and often partially infected needles will display a black demarcation line between healthy and diseased tissue. Eventually most needles in a portion of the branch may be infected and die. In general, dead needles remain attached to the branches. Basal sprouts of redwood can sometimes be girdled, cankers will appear as a dark lesion, and the entire portion of the sprout above the lesion will desiccate.
Symptoms ListTop of page
|abnormal leaf fall|
|yellowed or dead|
|canker on woody stem|
|discoloration of bark|
|gummosis or resinosis|
|plant dead; dieback|
|uprooted or toppled|
Biology and EcologyTop of page
Our understanding of P. ramorum is still limited and subject to be modified in the future. For reviews on current knowledge, refer to Rizzo et al. (2005), Sansford et al. (2009), Kliejunas (2010) and Grunwald et al. (2011).
The coastal distribution of the disease caused by P. ramorum (Rizzo et al., 2005) in California, USA, suggests that the pathogen is favoured by moist and moderate climates. Moisture in the infested region is provided both by precipitation and fog, and temperature fluctuations are relatively small when compared with the interior of California. Experimental evidence has indicated that infection of bay (Umbellularia californica) leaves is optimal when a film of free water remains on the leaf surface for at least 9-12 hours and temperatures are approximately 18°C (Garbelotto et al., 2003). These conditions are frequently met in the fog-drenched coastal region of California, where up to over 200 days of fog per year have been recorded. Within the coastal region, eastern and southern slopes are significantly drier. A comparison of inoculum viability between these dryer areas and the more mesic areas within the same region has indicated a much more pronounced seasonal pattern in drier climates (Davidson et al., 2002c). These observations, combined, indicate that maximum disease progression is to be expected in mesic areas with moderate climate.
In the absence of free water, plant infection is significantly reduced. It has been presumed that zoospores are the main source of infection. The most important feature of this forest Phytophthora is that all plant parts affected by the disease are aerial. Is this an aerial Phytophthora? There is no doubt that an aerial phase has to be invoked to explain the epidemiology of Sudden Oak Death. Sporangia are extremely deciduous and are produced in abundance on leaves and sometimes twigs of hosts such as bay laurel (U. californica) and tanoak (Notholithocarpus densiflorus). Infections can vary greatly from extremely abundant on almost every leaf in the lower and mid crown of bay trees in infested areas to just a few leaves, and sporangia can be recovered from rainwater. The extent of the aerial spread of P. ramorum is still unclear. In California the disease is always correlated to the presence of two species, bay laurel and tanoaks. In areas where tanoaks and California bay laurel coexist, infection of the latter tree species precedes and overwhelmingly surpasses infection of tanoaks, suggesting a key role played by this species in the epidemiology of the disease. After the first few rains, P. ramorum can be detected in the environment (soil, rain traps) (Davidson et al., 2002c). Leaf infection will occur in a few hours, and infected leaves may persist on the branch for more than a year, providing a persistent source of inoculum on some trees. When relative humidity is high, sporangia and chlamydospores will be produced on the infected leaves and will be splashed by rain onto other leaves and into the soil, and may become airborne. In hosts like tanoaks, foliar infections are often associated with twig infection: the outcome is twig and branch dieback. Oaks and the main stems of tanoaks are probably infected in a final stage of the disease. Sporangia are the most effective infectious propagule, presumably because they release the motile zoospores. Girdling cankers will proceed at varying rates, probably mostly affected by the genetic makeup of the individual infected tree. Variations in susceptibility to the pathogen have been noticed in both bay laurel and oaks. Susceptible individuals will potentially be girdled in just a few weeks. Girdled trees will look apparently healthy for several more months, until all resources have been depleted and the trees undergo a rapid decline. Resistance in tanoak has been identified (Hayden et al., 2011).
Soil and leaves may be infectious and highly contagious: it is possible to experimentally infect leaves by placing them over infested soil, and it is possible to infect wood by placing it under infected leaves. Conversely, it is extremely difficult to infect leaves by placing them near or on infected wood. These results indicate that leaves (including twigs) and not wood play a crucial role in the epidemiology of the disease. Because oak leaves are not generally infected by P. ramorum, oaks may not effectively spread the disease. In support of this hypothesis, surveys have indicated that oaks are much more likely to become infected by P. ramorum if they grow in proximity to bay laurel trees (Kelly and Meentemeyer, 2002; Swiecki and Bernhardt, 2002).
Sporangia can survive for several weeks even if dried, whereas the survival period for chlamydospores is still unknown. Chlamydospores are found in abundance in soil, streams and embedded in leaves. Chlamydospores embedded in bay leaves are quite resilient and will survive for a week with a constant temperature of 55°C. Both of these propagule types are potential means of long-range spread of the disease.
Genetic analysis shows P. ramorum infection occurs only in Europe and parts of North America, three clonal lineages have been identified: EU1, NA1 and NA2, named for the continent where they were first found, followed by a number indicating order of discovery (Grunwald et al., 2009).
Notes on Natural EnemiesTop of page
No natural enemies are known.
Means of Movement and DispersalTop of page
Natural dispersal of P. ramorum is by drifting plant material, waterborne and soilborne chlamydospores, and by waterborne, soilborne and wind-blown rain containing sporangia.
There are no known vectors of the disease other than man but any animal that can move soil is potentially a vector. P. ramorum has been proven to be effectively moved through the trade of ornamental plants and green waste. There is evidence that mature compost will not be infectious.
Pathway VectorsTop of page
|Clothing/footwear and possessions||Soil on clothing and equipment|
|Land vehicles||All if soil moved.|
|Soil, sand, gravel etc.||Yes|
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Bark||hyphae||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Growing medium accompanying plants||sporangia; spores||No||Pest or symptoms usually invisible|
|Leaves||fruiting bodies; hyphae; plasmodia; sclerotia; sporangia; spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Seedlings, Micropropagated plants||fruiting bodies; hyphae; plasmodia; sclerotia; sporangia; spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Stems (above ground), Shoots, Trunks, Branches||fruiting bodies; hyphae; plasmodia; sclerotia; sporangia; spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Wood||hyphae||Yes||Pest or symptoms usually visible to the naked eye|
|Plant parts not known to carry the pest in trade/transport|
|Bulbs, Tubers, Corms, Rhizomes|
|Flowers, Inflorescences, Cones, Calyx|
|Fruits (inc. pods)|
Wood PackagingTop of page
|Wood Packaging liable to carry the pest in trade/transport||Timber type||Used as packing|
|Loose wood packing material|
|Solid wood packing material with bark|
|Solid wood packing material without bark|
|Wood Packaging not known to carry the pest in trade/transport|
|Processed or treated wood|
Economic ImpactTop of page
The overall economic impact of P. ramorum in California, USA, is hard to assess. Californian oaks (Quercus spp.) and tanoaks (Notholithocarpus densiflorus) affected by the pathogen are not commercial timber species. The addition of redwood (Sequoia sempervirens), Douglas fir (Pseudotsuga menziesii), grand fir, red fir, western hemlock and other conifers as reported hosts poses a potential economic cost to the timber industry. Symptoms and impact on these hosts are somewhat limited, mortality is only reported from small (less than 1 inch diameter) trees. Dead tree counts are probably in the millions, but the extreme patchiness and wide extent of the disease makes any assessment of tree mortality extremely difficult (Kelly and Meentemeyer, 2002; Meenetemeyer et al., 2008). Oaks in particular are known to increase the real estate value of property: large numbers of landscape oaks have been infected, with significant financial repercussions for property owners. A decrease in property values has been shown in areas near infected forests in Marin County (Kovacs et al., 2011a, b). Mortality of oaks is likely to have doubled and that of tanoaks quadrupled (Swiecki and Bernhardt, 2001; McPherson et al., 2002) due to this disease. Costs of removal of dead trees and of disposal of the infectious green waste are also significant. The need for precautionary and sanitary practices is an added indirect cost to arborists and other tree professionals.
In 2009, P. ramorum was confirmed as the cause of extensive dieback and mortality in mature and juvenile Japanese larch (Larix kaempferi) at a number of sites in south-west England. In 2010, P. ramorum was isolated from larch plantations displaying similar symptoms in south Wales. Overall, 2400 ha or ca. 0.6 million mature larch were affected (Webber et al., 2011) in addition to a large area of juvenile larch. This is the first widespread and lethal damage caused by P. ramorum to a commercially important conifer species anywhere in the world. Additional highly valaued specimen rhododendron plants in historic gardens have been removed to maintain phytosanitary conditions.
Some industries have been particularly affected by P. ramorum, including the ornamental plants industry (Linderman et al., 2002; Parke et al., 2002) and the composting industry (Garbelotto, 2003). It is not only Californian growers that are affected, but also those outside California due to the decreased availability of Californian-grown propagative material. Edible mycorrhizal mushrooms are reported to have decreased in numbers in areas highly affected by the disease. Economic impacts in Oregon were estimated by Hall and Albers (2009).
Death of large numbers of trees in popular parks and recreation areas, and the partial closure of some infested areas during the rainy season, are having an impact on the recreational value of open spaces. The cost of tree removal and disposal for agencies, public or private, running large open spaces can be extremely high. The need to lower the risk of spread in industries affected by Sudden Oak Death will translate into management practices with a significant price tag (e.g. the washing of logging trucks, the closure of some roads and accesses, the need to process bay leaves to ensure the pathogen is dead, the need to ensure mature compost does not become contaminated by the green waste in fresh compost piles, and so forth). These expenditures can be considered indirect economic costs of P. ramorum.
Kliejunas (2010) reviewed P. ramorum economic and environmental impacts. Sansford et al. (2009) reviews economic impacts in Europe.
Environmental ImpactTop of page
Oaks and tanoaks are extremely susceptible to the disease. Tanoak (Notholithocarpus densiflorus) is the most susceptible species in California, USA. Some local populations, e.g. some canyons in the Big Sur area (Monterey County), have lost all of their adult trees because of Sudden Oak Death (SOD). The disease has the potential to cause a significant genetic bottleneck in this tree species. The demise of entire tanoak populations is changing the nature of those forests, in general moving towards pure redwood (Sequoia sempervirens) stands with marginal presence of oaks and Douglas firs. Wildlife depending on tanoaks is likely to be locally affected. Tanoak is also the major ectomycorrhizal host of most of these stands and its disappearance is likely to have a significant impact on ectomycorrhizal populations. Abundance of dead and fallen woody material constitutes a significant fire hazard (Cobb et al., 2011); it is likely that the intensity of these fires may be much higher than the norm because of the large accumulation of woody debris. The arrangements of fuels is altered, posing serious challenges to firefighter response in infested stands (Valachovic et al., 2011). The presence and incidence of coast live oak (Quercus agrifolia) is also bound to change, and some local strong shifts towards Douglas fir forests may be observed. The extremely adaptable and drought-resistant woodlands dominated by coast live oaks, are much more resilient than Douglas fir stands to prolonged periods of drought. While almost 100% of tanoaks have died in the worst-hit localized areas, rates of mortality for coast live oak are much lower, not exceeding 40% (McPherson et al., 2002). In spite of this, the amount of tree cover has decreased significantly in some areas affected by SOD. This reduced cover enhances the potential for erosion and for the establishment of undesirable plant species, including non-natives. Finally, P. ramorum may have a detrimental, but more subtle, effect on hosts other than oaks and tanoaks. Infected trees may be more susceptible to decline in the event of the onset of unfavourable climatic or ecological conditions. P. ramorum may also significantly affect the regeneration of some host species: by reducing overall seed productivity (killing mature plants, causing branch dieback) and by directly killing seedlings.
DiagnosisTop of page
P. ramorum will grow on most media used for other Phytophthora species such as cornmeal agar, PDA (not optimal), V8 and carrot agar (Werres et al., 2001). It grows relatively well between 15 and 22°C, but slows down significantly when temperatures go over 25°C. The most widely used selective medium to isolate P. ramorum from infected plants is corn meal based PARP (Rizzo et al., 2002a). While colonies will generally emerge from plated plant material within 6 days, at times up to 3 weeks has been necessary to obtain cultures. Cultures can be obtained from the following substrates: canker margins from oaks (Quercus spp.) and tanoaks (Nothorlithocarpus densiflorus), rhododendron leaves and stems, bay (Umbellularia californica). It is harder to isolate the pathogen from Rhamnus, Pseudotsuga, Arbutus or Heteromeles. From hosts such as Arctostaphylos, Acer, Aesculus and Lonicera, isolations can be extremely difficult. In California, a state characterized by an extremely marked Mediterranean climate, isolation success of P. ramorum follows a seasonal pattern, a trait not uncommon among Phytophthora spp. Isolation success tends to be best during late winter and spring, while it progressively declines as the dry California summer progresses. Almost every host has some specific requirements to maximise isolation success. The length of time that has passed between sample collection and processing has been shown to strongly affect the sensitivity of culture-based diagnostic methods (Vettraino et al., 2010).
For some foliar hosts, such as Umbellularia and Rhododendron, incubation in a moist chamber for 48 to 64 hours results in abundant sporulation. Sporangia and chlamydospores can then be analysed.
It is possible to bait P. ramorum from soil, streams, infected leaves, and to a limited extent from wood (Davidson et al., 2002c; Werres et al., 2001). The most common baits used for P. ramorum are pears, and 'Cunningham White' rhododendron leaves. Baiting is normally done for 5-7 days, and appears to be facilitated by temperatures between 12 and 15°C, at least for some substrates such as wood. Baits are collected at the end of the baiting period, left to dry for a couple of days, and then plated on selective PARP medium and incubated at 18°C. From mid-summer on, baiting from soil becomes unsuccessful. It is unclear whether this corresponds to a temporary dormancy period of the pathogen, or whether viability of the inoculum may be permanently lost. In infested areas it is possible to bait P. ramorum directly from the air by using healthy susceptible foliar hosts such as rhododendrons.
There is a wide selection of DNA PCR-based protocols to identify the pathogen both from cultures and directly from infected plant material (Garbelotto et al., 2003). A nested PCR approach is needed to obtain a signal from most foliar hosts with the exception of bay and rhododendron leaves. Because of the difficulty in isolating the pathogen from most foliar hosts, it is recommended to back up diagnosis based on isolations, with PCR-based data. Vettraino et al. (2010) concluded that a combination of either culturing and molecular diagnosis, or of two molecular assays was the most successful approach to identifying P. ramorum.
Tomlinson et al. (2005) developed a sensitive and specific single-round real-time PCR (TaqMan) assay using a portable real-time PCR platform. This has the advantage of being able to diagnose P. ramorum entirely in the field, independent of laboratory facilities.
Diagnostic methods are reviewed in Kliejunas (2010). For the USA, diagnostic and sampling protocols for official regulatory confirmations are posted at the USDA Animal and Plant Health Inspection Service (APHIS) P. ramorum website http://www.aphis.usda.gov/plant_health/plant_pest_info/pram/protocols.shtml#diag. A duplex PCR detection method, based on the internal transcribed spacer (ITS) regions of the ribosomal DNA, was developed by Schlenzig (2011) to enable sensitive detection of P. ramorum and to distinguish it from the similar P. kernoviae. Chimento et al. (2012) developed a real-time RT-PCR which is able to clearly distinguish between dead and viable P. ramorum pathogens.
Detection and InspectionTop of page
P. ramorum is difficult to diagnose from dead trees, even if death has occurred recently. Looking around the dead tree for trees with obvious symptoms (see Symptoms section) that are still green is recommended. Bleeding can be an easily visible symptom, but it can be due to a myriad of causes including mechanical wounding, cracking, insect attack and wood decay. Using a blade, cut the outer part of the bark and check for discoloration under it. A P. ramorum lesion may or may not have a clear zone line, but it will almost never have a regular shape. Borders are in general angular, and shape is often irregular. It is essential to uncover the border of the canker in order to diagnose a tree as infected by P. ramorum. Cultures should also come from the margin of the lesion (see Diagnostic Methods).
Bleeding is not always associated with cankers, and is normally absent in small tanoak (Notholithocarpus densiflorus) branches. In these cases, cankers will be visible as slight depressions in the bark, often appearing slightly water-soaked. A dark-brown or black lesion, without zone lines, will be present under the bark.
For all other hosts, inspection for leaf and branch symptoms is the first step. In rhododendron, look for both leaf blight and branch cankers. The two are often connected, so it will be possible to follow a lesion from the leaf into the bearing stem, and vice-versa. Lesions on rhododendrons often have diffuse margins, or conversely, dark lines in a concentric pattern highlighting growth patterns of the pathogen. Visible branch dieback is normally seen as a second stage of infection.
In the case of Umbellularia foliage, there is a good correspondence between the side of the leaf carried downwards and location of the P. ramorum lesion. This is due to the fact that swimming zoospores (requiring free water) are the main infection propagule responsible for foliar infections. If leaves are carried sideways, lesions will develop on the lower blade; if they are carried with their tip downwards, lesions will develop on the leaf tips, and so forth.
In California, USA, the most valuable diagnostic approach is to focus not on one tree but on an entire area. The diagnosis is strengthened by identifying a few different hosts, each displaying their characteristic symptoms.
Similarities to Other Species/ConditionsTop of page
Symptoms on plants are fairly generic and can be easily confused with those caused by other Phytophthora species, or with other fungal diseases. Culturing or molecular diagnostics need to be used to confirm pathogen presence.
P. ramorum cankers are in general above ground and do not develop in the roots: this feature can be helpful, but at times other Phytophthora species also cause aerial cankers. Lesions on Umbellularia resemble symptoms caused by bay anthracnose and by other Phytophthora species recently isolated in California and Oregon, USA (Davidson et al., 2002b). The lack of fungal reproductive structures can assist in differentiating P. ramorum symptoms from other symptoms caused by fungi. On Rhododendron spp., symptoms are identical to those caused by species such as Phytophthora cactorum, P. citricola, P. citrophthora and P. nicotianae for twig symptoms, and P. syringae for foliar symptoms (Werres et al., 2001).
Prevention and ControlTop of page
Removal of California bay laurel and treating with phosphonate, planting non-susceptible species and other strategies are being developed to prevent or manage P. ramorum in wildlands (Lee et al., 2010; Swain and Alexander, 2010). Best management practices for P. ramorum are available at: http://www.suddenoakdeath.org/diagnosis-and-management/best-management-practices/.
It has been shown that fresh wounds will be optimal infection courts. In restoration projects, avoid bay laurel (Umbellularia californica) if possible, especially in areas where oaks may be growing. Eradication has been attempted in southern Oregon, USA, via the burn-and-slash technique (Goheen et al., 2002b).
Knowledge to support a complete control programme is still limited; however, significant results have been achieved, considering the relatively short period of time since the pathogen was discovered:
- Kiln drying: 55°C for 30 minutes was insufficient to kill the pathogen. At least 1 hour required.
- Composting following guidelines prescribing piles to be kept at 55°C for at least 2 weeks is successful in eliminating the pathogen (oospores not present).
- P. ramorum is susceptible to label-dosages of copper sulfates and copper hydroxides. In different formulations it is moderately susceptible to mancozeb. The pathogen is sensitive to phosphites or phosphonates. Phosphite injections are effective in oaks and tanoaks (Notholithocarpus densiflorus). Phosphite foliar sprays are not effective on oaks and tanoaks. The pathogen is extremely sensitive to metalaxyl, but drenches and foliar sprays are ineffective in oaks (Garbelotto et al., 2002b).
- Water and moisture management are extremely important, especially when temperatures are between 15 and 20°C. Infection on bay (Umbellularia californica) leaves requires 9-12 hours of leaf wetness.
- Natural contagion from oaks is estimated to be low: susceptible oaks should not be planted near foliar hosts like bays and rhododendrons.
- Early infection can be detected on foliar hosts: new infection on bay leaves are good signs of inoculum level.
- Sites, soil and streams can be monitored by baiting by baiting with rhododendron leaves (Davidson et al., 2002c).
ReferencesTop of page
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ContributorsTop of page
09/03/12 Updated by:
Susan J. Frankel, Sudden Oak Death Research, USDA Forest Service, Pacific Southwest Research Station, Berkeley, California, USA
Top of page
- = Present, no further details
- = Evidence of pathogen
- = Widespread
- = Last reported
- = Localised
- = Presence unconfirmed
- = Confined and subject to quarantine
- = See regional map for distribution within the country
- = Occasional or few reports