Disease names always seem to be a bugaboo. This was an awesome disease name when this new, introduced pathogen started killing oaks and tanoak. Suddenly. Then it became apparent that other trees mainly get foliage infection, and are not killed. Hmm. Then when we found out it attacks a variety of shrubs and other plants, ‘SOD’ was often dropped in favor of ‘ramorum blight’, unfortunately including the specific epithet of the pathogen (until that changes).
Here SOD is grouped with the cankers, based on its effects on the first known hosts. But now we know that on some hosts the pathogen also can cause foliage disease and shoot blight.
As of 2013 (when USDA last updated its list), there were 47 regulated hosts (hosts proven by Koch’s postulates). In 2002 there were only 29. Moreoever, several of the hosts (Camellia, Kalmia, Pieris, Rhododendron, Viburnum) are listed only as genera, and include all species, hybrids and cultivars. An additional 92 plants are considered associated hosts (hosts strongly indicated by isolation or molecular test; up from 31 in 2002 and 58 in 2006). A complete host list can be downloaded from USDA Animal and Plant Health Inspection Service here. Hosts include the following:
- Some trees are very susceptible and are killed by spreading stem cankers:
- Tanoak (Notholithocarpus densiflorus) is highly susceptible and trees of all sizes are rapidly killed. All above-ground parts can be infected.
- Oaks in the red oak group, coast live oak (Quercus agrifolia), California black oak (Q. kelloggii) and shreve oak (Quercus parvula var. shrevei) are commonly infected on the main stem and large branches and killed from such cankers. Canyon live oak (Quercus chrysolepis), in a small group of intermediates between white and red oaks, is also a known host.
- Other tree species suffer mostly a foliage infection:
- California bay laurel (Oregon myrtle, Umbellularia californica) is a foliar host. Lesions commonly occur on leaf tips.
- Big leaf maple (Acer macrophyllum)
- Madrone (Arbutus menziesii). In addition to foliage infection, madrone may get branch and stem cankers severe enough to kill the tree.
- Manzanita (Arctostaphylos spp.)
- California buckeye (Aesculus californica)
- Victorian box (Pittosporum undulatum), a small ornamental tree in the San Francisco Bay area, has been found with leafspots caused by the pathogen.
- Cascara buckthorn (Rhamnus purshiana) may suffer shoot dieback as well as foliar infection.
- The two most alarming additions to the host list are among the most treasured and valued tree species of the Pacific coast. However, occurrence of the disease on these hosts is limited in distribution and severity, and no symptoms have been seen on overstory trees. Disease on these hosts may be restricted to areas with very high inoculum (because of more susceptible species, especially bay laurel) and especially conducive environment:
- Coast redwood (Sequoia sempervirens) was reported as a host based on isolations from discolored leaves and small branch cankers on saplings in two locations in California, as well as molecular analysis of dying basal sprouts from five other locations . Inoculation tests confirmed pathogenicity to redwood.
- Douglas-fir (Pseudotsuga meziesii) was reported as a host based on isolations from saplings with small branch cankers and branch dieback in one area in Sonoma County in coastal California . The EU1 lineage as found in Oregon attacking Douglas-fir and grand fir (Abies grandis) .
- Many understory species also are affected, showing foliar lesions and stem cankers. These include:
- Rhododendron spp.
- Huckleberry (Vaccinium ovatum). Stem cankers and shoot dieback.
- California honeysuckle (Lonicera hispidula). Leaf spots.
- Toyon (Heteromeles arbutifolia). Leaf spots, branch dieback.
- California coffeeberry (Rhamnus californica). Leaf spots.
- Western starflower (Trientalis latifolia), a herb, leafspots with yellow halo.
- Poison oak (Toxicodendron diversilobum) was found to be susceptible by Everett Hansen (you’re a better man than I, Gunga Din) . Unfortunately it is rarely killed.
- Salmonberry (Rubus spectabilis). Leaf and shoot blight in southwest Oregon.
- California hazel (Corylus cornuta var. californica), a large shrub or small tree.
- In addition, many other species that occur outside the current distribution of the disease, such as northern red oak, are susceptible in seedling inoculations.
The pathogen was a new species , Phytophthora ramorum, a member of the Oomycota. It produces at least two kinds of spores:
- chlamydospores, which are resistant and probably not independently dispersed except with plant matter or soil; and
- sporangia that, unlike those in most Phytophthora species, can be deciduous and can germinate directly to infect plants, potentially functioning as airborne conidia as in Phytopthora infestans, the cause of late blight of potato. The sporangia may alternatively give rise to swimming zoospores.
Oospores have not been found in nature, though they may occur. Oospores have been produced in culture by pairing naturally occurring A1 and A2 mating types, both of which occur in Europe.
Sporulation is prolific on foliage of Umbellularia californica during moist winters, and this source of inoculum tends to drive epidemics . Survival in foliage over the dry summer is best with dense canopy cover and temperatures below 30 C. The pathogen has a temperature optimum of 15-20 C. The prevalence of the disease in coastal areas is likely related to moisture and cool temperatures that facilitate sporulation and survival.
The pathogen presumably survives periods unsuitable for growth as mycelium, chlamydospores or as oospores.
Strangely, sporulation has not been detected on stem and branch cankers and must be rare if it occurs at all. Thus, the lethal disease on woody hosts apparently does not contribute to inoculum. Hosts that get lethal cankers likely are infected by inoculum produced on foliar hosts, especially Umbellularia californica. Abundant sporulation has been found on foliar lesions in the field and can readily be induced on lesions in the lab. Lesions on leaves dried for several months under mild temperatures can still sporulate.
The pathogen may enter new areas when soil is carried on vehicles or animals or perhaps when infected host material is carried into new areas. The soilborne phase may be mycelium, chlamydospores and perhaps oospores in infested host material, or spores in soil. Inoculum may also be carried in streams. It is most commonly detected by placing a leaf of a highly susceptible host, such as Rhododendron, in the stream as bait.
The pathogen has been found in soil and may be soilborne but infections are exclusively on above-ground plant parts; the fungus does not infect roots. Experimental inoculations indicate that infection can occur without wounding, both on leaves and stems.
- In some hosts, only leaf infections occur, resulting in irregular lesions and spots.
- In others, cankers occur on large branches and stems (see Hosts above). Plant mortality usually occurs from cankers, which are diffuse and develop rapidly. Bark may discolor, appear watersoaked, and/or bleed dark liquid at the margins. Dark lines often occur in the inner bark. Discoloration only goes a few millimeters into the wood.
- In Douglas-fir and coast redwood, symptoms are restricted to small saplings and to sprouts in the case of redwood, consisting largely of foliar lesions, branch cankers, and resulting branch dieback [7, 16].
As stems die, succulent shoots may wilt and leaves turn brown. Mortality may precipitate or be accompanied by attack by ambrosia beetles, oak bark beetle, the saprot ascomycete Hypoxylon thoursianum, and Armillaria species coming up from the roots.
There is no root infection and cankers do not extend below the soil line.
California. The disease was first reported in 1995 in Mill Valley, Marin County, just north of San Francisco. It is now confirmed in 15 counties of California, from Monterey County in the south to Humboldt county, well into northern California . However, this does not include detection of the pathogen in plant nurseries, which has occurred in Los Angeles area and elsewhere. The featured image above shows the disease in hills of Big Sur, California.
Oregon. The disease was found in southwestern Oregon in 2001. Near Brookings, in Curry County, Oregon, a number of infection foci were found over an area of nine square miles. An eradication campaign was quickly organized, involving cutting and burning all vegetation in and near the foci. During this process additional foci were discovered and treated. Discoveries continued, however. The pathogen can survive cutting and burning of infested areas. Now treatments include herbicide to prevent sprouting, which can carry the disease, or repeated cutting and burning until no inoculum can be detected. Eradication has proven largely unsuccessful.
How the fungus made such a large jump (if indeed the forests between Oregon and the California infestation are not more or less continuously infested) is not clear. This disease seems to be spreading as fast as any disease introduced to North America thus far. If there is any reason for optimism at all, it is that, thus far at least, the disease seems to be restricted to coastal areas.
As of 2017, Curry County had a “Generally Infested Area” of 150 km2 (58 mi2), included in a Quarantine Area of 1344 km2 (519 mi2) [1, 2]. These areas have expanded greatly over time, and the Quarantine Area is starting to look generally infested .
A recent development in Oregon is the apparent leaking of the EU1 lineage from nurseries into natural forests [1, 2]. EU1 was first found in 2015 and has expanded to 134 ha in 7 sites. Eradication efforts are now focused on EU1.
In 2021, the NA2 lineage was found in natural forests for the first time, 20 miles north of the quarantine area in Oregon . Previously it was known only from nurseries.
The pathogen has been found repeatedly causing foliar symptoms in various nurseries and even in landscape plantings in northern Oregon. Genetic evidence suggests that eradication efforts may be successful in nurseries, but the pathogen is reintroduced frequently [19, 20]. The genotypes were not the same as the wildland isolates in Curry County, until EU1 appeared, first in nurseries and then in wildlands.
Washington. The first detection in Washington was 2003, when the pathogen was found on rhododendron in a nursery in King County, then in Pierce County. Presumably the infestations arose from the infested nursery stock shipped from southern California. Despite eradication attempts, the nurseries continued to test positive. Then the pathogen was found in a stream draining a nursery, then on rhododendron in a third nursery in Pacific County. It continues to pop up in nurseries and streams.
In 2015, a small infestation was found in the Kitsap County Botanical Garden. As of 2017, eradication efforts appear to have succeeded.
British Columbia. Just as in Washington, in June 2003, the pathogen was found on rhododendrom at a nursery outside Vancouver, British Columbia. Detections continue occasionally in the Vancouver area.
Elsewhere in North America. In early 2004, the disease was found in Monrovia Nursery near Los Angeles, California. This large production nursery ships extensively throughout the United States. Traces of shipments, and surveys in the target states, soon revealed that the disease was present in nurseries in many other states, primarily in the South.
Other than the Pacific Coast, there is no evidence that the pathogen has become persistently established in the wild in any of these states. However, occasional detections continue in nurseries, streams, and even landscape plants around businesses and homes . Detection of established populations in the wild may be just a matter of time.
Aside from the California and southern Oregon coasts, studies of risk in the US suggest that the Appalachian Mountains and portions of the Gulf Coast also have a highly suitable combination of hosts and climate for the disease . Such areas are of particular concern for disease spread.
The pathogen itself was discovered and described in the Netherlands  at about the same time that the etiology of sudden oak death was being elucidated in California. In Europe the pathogen had been most common in nurseries and gardens on rhododendron and viburnum. In 2003, the pathogen was found infecting European beech, southern and northern red oak, Holm oak, and horse chestnut trees in the Netherlands and UK. In all cases, the trees were near infected rhododendron.
The pathogen is now widespread in Europe. In forests, at least in Britain, the invasive shrub Rhododendron ponticum is a common host [18, 21], and provides most of the inoculum for lethal infections of trees, much as U. californica does in California and Oregon .
In 2009, Larix kaempferi (Japanese larch), an important plantation timber species, began to be affected in the British Isles. The pathogen sporulates prolifically on larch needles, so it does not depend on R. ponticum for propagation. At least in southwestern Scotland and across the sea in Northern Ireland, these attacks are due in part to the newer EU2 lineage as well as EU1 . It has resulted in mortality or forced premature harvest of millions of larch. Japanese larch is also attacked in France.
Realistically, little or nothing can be done to treat infected plants or protect plants from inoculum. An experimental effort to stop local spread in generally infested areas is being conducted in northern California; this consists of removing bay laurel and tanoak, followed by pile and broadcast burning. However, most effort is directed at limiting the spread of the disease into new areas, particularly because the evidence available suggests that eastern oak species are just as susceptible as California oak species in inoculations [10, 11].
- Avoid movement of infested material. To a large extent this is done through quarantines.
- Probably all of the long-distance movement of this pathogen has been through nursery stock. We could have prevented spread from California by prohibiting all movement of potentially susceptible plants. In fact we could have stopped its introduction, and could prevent similar introductions in the future, if we prohibited all international trade of plants except for carefully selected propagation materials. Economically, this is considered unacceptable by the government.
- Harvesting of all potential host materials should be stopped in and near infested areas. This includes firewood, fuelwood, timber, transplants, fruits and seeds, greenery, etc. Because plant parts may be hard to identify, in many cases this ban should be expanded to broader groups of plants and plant parts.
- Soil movement from infested areas should be curtailed. No soil should be collected, vehicles should be thoroughly washed after off-road travel, and hikers should wash their shoes.
- The European Union adopted a quarantine against the pathogen on November 1, 2002. This affects export of susceptible plants from the United States and other countries known to have the pathogen as well as transport of plants within Europe.
- Active surveillance is needed to detect new areas of infestation.
- In California and Oregon, intensive surveillance is underway to detect new areas of infestation. New areas will be included in quarantines.
- The U.S. Forest Service and the Animal and Plant Health Inspection Service are organizing a national survey for early detection of new areas of infestation. The survey will include nurseries that deal in potentially susceptible plants and nearby forested areas with potentially susceptible plants, especially where the moisture regime is suspected to be conducive.
- When new infestations are found, far from the previously known range, eradication is attempted.
Lineages and mating types. Using molecular phylogenetics, four clades, or lineages, have been found within the species Phytophthora ramorum. The differ slightly in biology, and will probably be described as formal taxa .
Lineages are named after the continent where first detected, followed by the number representing its order of discovery on that continent: EU1, EU2, NA1, NA2. NA1 arrived in North America on nursery shipments some around 1990 or earlier . NA2 was later found in nurseries in California, Washington and British Columbia. EU1 was first found in Germany and the Netherlands, but it spread to the UK and elsewhere, including North America. It occurs on various hosts, but the greatest damage has been to Larix kaempferi (Japanese larch), which is a major commercial plantation species. In 2013 it was reported in nurseries and streams in Washington and California. In 2015 multiple infection loci of EU1 were found in southwest Oregon. EU2 is known to be in Northern Ireland and Scotland.
Analyses revealed no evidence for sexual recombination; the variation observed appears to be due to somatic recombination or mutation. The population in US forests appeared to be almost completely derived from a single introduction. Populations in nurseries, both in North America and in Europe, have more genetic diversity, suggesting that introductions and movement of P. ramorum in nurseries, occurring via trade of infected plant material, have been more frequent than in forests.
In Oregon, the forest population has been dominated by a single genotype that persisted over the years despite eradication efforts, suggesting that eradication has not completely eliminated inoculum sources . Nursery populations have been more diverse, including even one genotype from the European lineage. That EU1 lineage has now been found in forest environments. Nursery populations appear to be eradicated successfully more often than those in forests, but they are also replaced with new introductions more often. Analyses indicate that “leakage” of nursery populations into forests have been rare to date [14, 19].
Members of the Oomycota are heterothallic with two mating types (designated A1 and A2); both are required for sexual reproduction. Regarding P. ramorum, originally only A1 mating type was found in Europe, and only A2 was found in North America. Now a few occurrences of the opposite mating types have been found on both continents . However, there is still no evidence that the fungus is reproducing sexually in nature.
Exotic? Sudden oak death (SOD) is a new disease that became established around the San Francisco Bay of California and has since been found in southern Oregon and Washington and more recently disseminated to other parts of North America.
Nursery stock is suspected as being the pathway of movement of the pathogen, although genetic evidence suggests that the population in California and that in Europe probably had separate origins. The native range of the pathogen is still unknown.
The fungus is almost certainly introduced to California, and the same species has been found in Europe, but the origin and nature of the introductions are unknown. Virtually all the facts point to a recent introduction:
- The disease was unknown until 1995.
- The disease is devastating, with little resistance in many of the native hosts.
- The disease rapidly expanded its distribution in North America.
- Genetic variation of the pathogen in North America and Europe is very limited [14, 19, 20], consistent with introduction of only a few genotypes.
- The pathogen has been found in Europe in nurseries and gardens. Infection of trees has been uncommon in Europe.
Extent of damage. Sudden oak death may develop into one of the most devastating diseases to hit North American forests, but this is uncertain. Some say its potential was overblown, it is killing relatively unimportant tree species, and doesn’t seem to be establishing itself away from the Pacific coast. Even in the 12 California counties that were invaded by 2004, however, the hosts that are readily killed are dominant on 1.5 million acres . The ecological and economic impacts of this pathogen worldwide are expected to be great [5, 9].
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