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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.
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).