- Infests plants in more than 70 genera; some are killed, others survive; some hosts support spread of the infection (see detailed descriptions below).
- Host species and genera include ashes, California bay laurel (Oregon myrtle), camellias, Douglas-fir, hemlock, huckleberries, larch, lilacs, Pacific madrone, magnolias, maples, mountain laurel, oaks, redwoods, rhododendrons, and viburnums.
- Phytophthora ramorum was probably introduced to North America on infected imported plants in the late 1980s or early 1990s.
Sudden Oak Death (SOD) first came to attention in the mid-1990s, when a large number of oaks and tanoaks began dying off in California’s coastal hardwood forests apparently victims of a then unknown disease. By the summer of 2000, the pathogen causing SOD was isolated, and was subsequently named Phytophthora ramorum. Since 2004, SOD has been recognized in 16 coastal California counties, from Monterey north to Del Norte, as well as in Curry County, Oregon (USDA APHIS memo, May 21, 2021). The principal spread of the disease has been within already infested areas.
In the affected Pacific coastal region, SOD has killed an estimated 50 million trees in California and Oregon. The preponderance are tanoaks (Notholithocarpus densiflorus): an estimated 29 – 44 million (1.6 – 2.5% of the species’ total population in California and Oregon) have been killed. Another 1.9 – 3.3 million trees belonging to one of two oak species – coast live oak (Quercus agrifolia) and Shreve oak (Q. parvula var. shrevei) have died (0.4 – 0.7% of their combined populations). Up to 1.1 million California black oaks (Q. kelloggii) have also been killed (less than 0.17% of their population).
California bay laurel (Umbellularia californica) is not killed by P. ramorum but instead drives spread of the outbreak in California. An estimated 91.4 million infected California bay laurel trees are present in the state.
These estimates are considered to be conservative because they are based only on trees that have been confirmed to be infected by direct, cultural isolation during a period up to 2014. In the intervening six years, the infection has intensified as a result of favorable weather patterns. An aerial survey in 2018 detected a large increase in tanoak mortality in counties California counties reaching from Mendocino south to Monterey (COMTF Report, September 2018).
When plants are small, or in instances where there is a heavy inoculum load, rhododendron, camellia, Pacific madrone (Arbutus menziesii), evergreen huckleberry (Vaccinium ovatum), and other hosts may also succumb to the pathogen. In addition, several conifers have been identified as hosts, although the impact of the pathogen on them remains unclear. In the US, these include coastal redwood (Sequoia sempervirens), Douglas-fir (Pseudotsuga menziesii), grand fir (Abies grandis), and Pacific yew (Taxus brevifolia). In the United Kingdom (UK), they include Japanese larch (Larix kaempferi) and western hemlock (Tsuga heterophylla – native to North America). In all, nearly 130 plant species are currently recognized by the US as hosts of P. ramorum; however, as the list can change, it is important to reference the USDA Animal and Plant Health Inspection (APHIS) website http://www.aphis.usda.gov/plant_health/plant_pest_info/pram/downloads/pdf_files/usdaprlist.pdf for the most current information. Many hosts do not die if infected, but rather act as sources of inoculum. Of those hosts that support inoculum production, California bay laurel and tanoak are considered to be the driving force of pathogen distribution in California and Oregon forests, with spores readily building up on the leaves and twigs, and then dispersing into the local environment.
In California and Oregon, some of these species are the dominant hardwoods over large areas, growing in nearly pure stands. P. ramorum is now known to infect nearly all of the major trees species in California’s infested counties. In Marin County, California, coast live oaks are becoming infected at a rate of 5% per year; they are dying at a rate of 3% per year (McPherson et al., 2010). Death of SOD-infested trees can be accelerated by attacks by bark and ambrosia beetles (McPherson et al., 2008; 2010). In sites heavily impacted by the disease, coast live oak is predicted to lose up to 70 percent of its basal area over the next 15 years (Brown and Allen-Diaz, 2009).
As of 2015, the pathogen was found in only about 10% of California’s forest area considered to be at risk. According to a model developed by Ross Meentemeyer (University of North Carolina, Charlotte), in the absence of any control efforts, the epidemic may increase ten-fold by 2030 along the coast, from the San Francisco Bay Area into Oregon. As noted above, the infestation intensified considerably following wet winters in 2016 and 2017.
The disease can affect even trees that are not highly vulnerable hosts. When SOD invades a tanoak-redwood forest, it not only kills the tanoaks – the principal hardwood /mast-bearing species in these forests. It also changes the fire dynamic in ways that damage the redwoods, also. The dead tanoaks provide more fuel for wildfires; the gaps created by their death also make the forests dryer. Finally, flames can reach the forest canopy by traveling up the standing dead tanoaks. This means that redwood trees’ crowns, which normally are out of reach of the fires, are scorched. The result is that the redwoods are killed at rates nearly four times those of un-infested forest plots.
Phytophthora ramorum is a non-native, invasive species in North America and Europe. It is believed that the pathogen was imported to both continents via the ornamental plant trade through several separate introductions from probably more than one unknown location. Through genotyping efforts, four clonal lineages have been identified – two in North America (NA1 and NA2) and two primarily in Europe (EU1 and EU2) – all of which likely diverged more than 100,000 years ago. At least five global migrations of the pathogen have occurred, with the NA1, NA2, and EU1 lineages being imported into North America, and the EU1 and EU2 lineage into Europe. It is believed that the US and Canada received the EU1 lineage unknowingly through importation from Europe. To date, the four lineages have not been found recombining in natural settings; however, there is still apprehension over their coexisting in one location at a given time, as a hybridized genotype could cause even more die-off and would further complicate suppression and containment efforts. Both the EU1 and NA2 lineages have been found in forests in Oregon (COMTF Report, June 2021).
There is concern that P. ramorum could become established in eastern North America, causing significant damage if the pathogen were introduced to the natural environment in a location where host plants and climatic conditions were conducive to pathogen viability. Many tree and shrub species native to the East Coast are hosts of the pathogen, as demonstrated by laboratory studies or natural infection of the species in plantings in Europe. Species of concern include northern red oak (Quercus rubra), chestnut oak (Q. prinus), white oak (Q. alba), pin oak (Q. palustris), sugar maple (Acer saccharum), black walnut (Juglans nigra), and mountain laurel (Kalmia latifolia). Of most concern is northern red oak as it has been found naturally infected in Europe and is highly susceptible in laboratory studies. Northern red oak is an extremely valuable wildlife food source and valuable for timber and oak veneer. Chestnut oak is also a concern as it has been found to be a susceptible stem and foliar species based on inoculation studies. This species is a dominant tree in the Piedmont and mountain regions, and its acorns are an important food source for wildlife. National risk maps are available based on both host presence and climatic variables favorable to the disease.
To determine pathogen viability in the eastern US, it is necessary to establish if there are host plants present that will support sufficient levels of pathogen sporulation. Research to date has found that mountain laurel may die too quickly once infected to support pathogen spread. While eastern rhododendrons have not yet been tested, rhododendrons are key sporulating hosts for the EU1 lineage of the pathogen in Europe. Tooley and Browning (2009) determined that a number of plants common in eastern deciduous forests are foliar hosts (hosts with a potential to support sporulation), including flowering dogwood (Cornus florida), sassafras (Sassafras albidium), black locust (Robinia pseudoacacia), black cherry (Prunus serotina); and two widespread invasive species, Japanese honeysuckle (Lonicera japonica) and multiflora rose (Rosa multiflora).
Disease management in the West
In California, the disease is now confirmed to be present in 16 counties, reaching from Del Norte in the north to southern Monterrey County in the South. As of early 2021, surveys have not detected SOD in San Luis Obispo County. Periodic wet periods have led to expansion and intensification of the disease in these areas. In autumn 2020, the EU1 strain was detected in Del Norte County; the source of the infection is unknown (COMTF Report, February 2021).
The Oregon outbreak was detected in 2001, in Curry County (southwest Oregon, just north of the California border). State and federal agencies there tried for a dozen years to eradicate outbreaks. They now focus on trying to slow the spread of the pathogen by early detection and treatment of outbreaks on the edge of the infestation. Periodic wet periods have led to expansion and intensification of the disease in Curry County, leading to repeated expansions of the quarantined area. Since detection of the EU1 strain in 2015, the highest priority has been assigned to eradicating those outbreaks. In addition, federal agencies continue to treat infestations on federal land. Finally, officials are encouraging logging of tanoak to reduce inoculum levels.
Currently, there are few options for managing SOD in the forest. One hopeful sign is that asymptomatic coast live oak trees persist in many heavily infected stands after more than 15 years of exposure to the pathogen. In addition, some trees have apparently recovered from infections. Experiments in the Wood lab at UC Berkeley and the Bonello lab at Ohio State University have shown that this apparent resistance is associated with individual trees’ production levels of four phenolic compounds produced by the tree’s phloem – so it is potentially durable (McPherson, et al. 2014).
Furthermore, a relatively simple and rapid means of identifying resistant coast live oaks appears to be on the horizon: chemical fingerprinting based on FT-IR spectroscopy of phloem extracts combined with chemometric analysis (Conrad et al. 2014).
Knowing which oaks are resistant (or susceptible) can guide homeowners, extension agents, and forest managers interested in protecting high-value trees with chemical treatments, protecting stands with high levels of resistance from development and fire, or for the development of SOD management and risk assessment plans [Conrad et al. 2014).
Preventing spread of P. ramorum to uninfested areas of the country
Several common nursery trade species, such as rhododendron, camellia, viburnum, pieris, and kalmia, are also P. ramorum hosts. Given the relatively recent identification of the pathogen, the steep learning curve associated with its discovery, and the great variability of symptoms on hosts, it is not surprising that the pathogen has been unknowingly shipped on nursery stock. Awareness of this risk exploded in the spring of 2004 when officials discovered the disease on camellias at a large California nursery that shipped $30 million worth of plants interstate on an annual basis. By the end of 2004, 176 nurseries in 21 states had received infected plants, 125 of which were linked to the California supplier.
After some states took unilateral action, the USDA Animal and Plant Health Inspection Service (APHIS) imposed an Emergency Federal Order on the interstate movement of nursery stock, cut greens, and other host plant material from California, Oregon, and Washington (Code of Federal Regulations: 7 CFR 301.92 – http://www.gpoaccess.gov/cfr/retrieve.html – URL goes to CFR website where current regulations can be retrieved by entering 7 as title; 301 as part; 92 as section into correct boxes and leaving year as most recent). Federal regulations were first implemented in 2002; however, prior to 2004, they only included the 14 infested California counties and the infested area of Curry County, Oregon.
These regulations have substantially reduced the presence of P. ramorum on nursery stock; however, they have not successfully eliminated it. Between 2003 and 2011, 464 nurseries in 27 states had tested positive for the pathogen, the majority as a result of having received infected plants from wholesalers. In 2012, 21 nurseries were confirmed as having infected plants; in 2013, 16 nurseries.
In August 2018, APHIS released proposed revisions to the regulation at http://www.regulations.gov/#!docketDetail;D=APHIS-2015-0101. The agency’s goal was to provide regulatory relief to West Coast nurseries that have not recently been found positive for P. ramorum while ensuring that the nursery trade does not spread the disease. The proposal’s components would formalize steps taken in a series of Federal Orders issued over the past decade. Only10 organizations commented.
Some commenters said that to prevent spread of the disease through the nursery trade, APHIS should not simply formalize existing practices but instead should strengthen the regulatory system by regulating all nurseries that ship P. ramorum host plants – regardless of their location or history of disease presence. Furthermore, inspections should be based on sampling and testing of soil, growing media, and water, rather than on visual inspection of plants. Furthermore, APHIS should update its list of host plant species to reflect scientists’ work since 2012. All the comments are available at http://www.regulations.gov/#!docketDetail;D=APHIS-2015-0101. The regulatory revision went into effect in May 2019.
Also in 2019 state authorities detected Phytophthora ramorum on plants entering their states. Over time, it was determined that 18 states had received plants possibly infected by the pathogen; positive plants were confirmed in seven states (COMTF Report, August 2019).
A major concern is the continuing presence of nurseries that have been found to have P. ramorum-positive plants more than one year, despite having carried out the USDA APHIS Confirmed Nursery Protocol (http://www.aphis.usda.gov/plant_health/plant_pest_info/pram/downloads/pdf_files/CNPv8.0-Oct-08.pdf). In such instances, it is often not clear whether the infestation has persisted or has been re-introduced to the nursery from another location. Genetic testing for the pathogen lineage would help to distinguish between repeat nurseries and new introductions; however, such rigorous analysis is not required. The pathogen can persist in plant material, water, soil, and growing media, including on recycled pots.
Another concern is the extent to which P. ramorum can escape infested nurseries (or diseased nursery stock planted in yards or other places) and cause disease in native plants. In some cases, vegetation outside infested nurseries has been found infected. One case occurred in Washington in 2009, when infected salal (Gaultheria shallon) plants growing on a stream bank outside an infested nursery were P. ramorum-positive water from the infested nursery area ran off into a stand of native salal. The salal has since been removed, and plans are under way to pave over the area. This was the first documented incident of P. ramorum moving out of an infested nursery and causing disease outside the nursery. APHIS began requiring testing of water inside infested nurseries in 2005; however, only nursery water used for irrigation is required to be cleaned up if the pathogen is found. Other water found onsite can remain contaminated, regardless of its threat to plants and the surrounding landscape if a flood were to occur. P. ramorum has also escaped from some nurseries into streams or ponds in Florida, Georgia, Alabama, Mississippi, North Carolina, and Texas. Whether the pathogen will spread further in these regions is not yet known.
The USDA Forest Service (FS) has been testing streams since 2006 as part of the P. ramorum of Forest Environments. In total, 320 unique watersheds have been surveyed. As of 2013, this survey has identified seven streams in Washington State, and 11 streams in the Southeast. Oregon and California operate their own, more extensive, stream survey programs. Oregon has never found P. ramorum in streams outside the Curry County outbreak area.
Nursery management practices are key to elimination of the pathogen in the ornamental nursery industry. There is agreement that the most effective program would rely on a critical control point strategy or systems-based approach using the best available science. In January 2014, APHIS issued a Federal Order that requires nurseries that test positive for P. ramorum to adopt APHIS-approved integrated management programs to address all the identified high-risk actions. For the first time, the agency will regulate based on testing of water, soil, and other potentially-infested articles in the nursery, not just the presence of diseased plants. [United States Department of Agriculture Animal and Plant Health Inspection Service. 2014. APHIS Revises Phytophthora ramorum Domestic Quarantine Regulatory Requirements for Certain Host Nurseries. January 10, 2014]
The European (EU1) and US lineages (NA1, NA2) of P. ramorum have different environmental and host preferences, and apparently different levels of virulence. The origin of the European strains, like the US strains, is from an unknown location; however, it is likely from a different source than the US source given the different lineage.
Before the pathogen was formally named, in Europe the pathogen was found on German nursery and landscape rhododendron plants in the mid-1990s. In 2004 it was found in nurseries in at least 11 European countries. By 2009, P. ramorum had been found in nurseries or gardens in 22 European countries, from Ireland and Norway to Poland and Serbia.
In autumn 2003, UK scientists detected the first cases of nearby trees becoming infected as a result of spores from outplanted nursery stock. By 2008, there were burgeoning reports of landscape outbreaks throughout Europe, with 14 countries affected; however, infected forest trees are still found only in the UK and Netherlands. Of the impacted European countries, the UK has had the greatest number of infestations, with more than 150 outbreaks in managed gardens, woodlands, or wild planting areas in England, Wales, and Scotland. Concern there over the health of ecologically valuable heathlands is great, as bilberry (Vaccinium myrtillus) is the dominant species, and it is highly vulnerable to the pathogen, as well as a good supporter of its sporulation. Four of the seven types of the world’s heathland occur in England, with the UK supporting approximately 75% of the total (global) upland habitat.
In spring 2009, the UK Government launched a 5-year program aimed at reducing P. ramorum and P. kernoviae inoculum to epidemiologically insignificant levels. Program components include removal of the principal sporulating host (the exotic plant Rhododendron ponticum) and the identification and control of any new outbreaks, helping to minimize the risk of further disease development or pathogen spread. P. ramorum and P. kernoviae research continues to improve understanding of the diseases they cause as well as to identify more effective control measures. To implement the 5-year program, £4 million was allocated for the first three years.
That same year, P. ramorum was found in mature plantations of Japanese larch (Larix kaempferi), infecting shoots and foliage, producing wilted, withered shoot tips, blackened needles, and branch dieback. Between 2009 and 2015, 8.5 million larch over nearly 22,000 acres were felled in an effort to contain the pathogen’s spread. Understory beech, birch, oak, and western hemlock have all been found with bole cankers. Some of the confirmed sites had little or no rhododendron present. Before 2009, tree infection in the UK has only been identified in relatively close proximity to infected rhododendron.
The first report of P. ramorum outside nurseries and ornamental settings in mainland Europe was detected in 2015 on larch plantations in France. Mortality rates are high: by May 2018, about 80% of the trees in the more infected plots in one set of larch plantations in Brittany (Northwest France) were symptomatic or dead. A second outbreak was a few kilometers away in a mixed forest stand of larch, oak and sweet chestnut (Castanea sativa) was less intense. Both stands have been removed (COMTF Report, September 2018).
For more information on P. ramorum and Sudden Oak Death, go to the California Oak Mortality Task Force website at www.suddenoakdeath.org.
An earlier version of this write-up benefited from significant input from Katie (Palmieri) Harrell, then with the California Oak Mortality Task Force.
Brown, L.B., and Allen-Diaz, B. 2009. Forest stand dynamics and sudden oak death: mortality in mixed-evergreen forests dominated by coast live oak. For. Ecol. Manage. 257, 1271–1280. doi: 10.1016/j.foreco.2008.11.030
COMTF Reports (e.g., August 2019, September 2018, February 2021, June 2021) can be found at https://www.suddenoakdeath.org/library/newsletter-archive/
Conrad, A.O., L.E. Rodriguez-Saona, B.A. McPherson, D.L. Wood, P. Bonello. 2014. Identification of Quercus agrifolia (coast live oak) resistant to the invasive pathogen Phytophthora ramorum in native stands using Fourier-transform infrared (FT-IR) spectroscopy. In Press; Frontiers in Plant Science.
USDA APHIS memo (May 21, 2021) sent to State and Territory Agricultural Regulatory Officials. Subject: APHIS Adds Del Norte County in California to Phytophthora ramorum Quarantine Area.
European Union. 2009. Risk Analysis of Phytophthora ramorum, a Newly Recognised Pathogen Threat to Europe and the Cause of Sudden Oak Death in the USA. http://rapra.csl.gov.uk/.
Frankel, S.J., J.T. Kliejunas, and K.M. Palmieri, technical coordinators. 2008. Proceedings of the sudden oak death third science symposium. Gen. Tech. Rep. PSW-GTR-214. Albany, CA: U.S. Department of Agriculture, Forest Service, Pacific Southwest Research Station. 491 p. Available online at: http://www.fs.fed.us/psw/publications/documents/psw_gtr214/.
Frankel, S.J., J.T. Kliejunas, and K.M. Palmieri, technical coordinators. 2010. Proceedings of the sudden oak death fourth science symposium. Gen. Tech. Rep. PSW-GTR-XXX. Albany, CA: U.S. Department of Agriculture, Forest Service, Pacific Southwest Research Station. In press.
Goss, E.M.; Larsen, M.; Chastagner, G.A.; Givens, D.R.; and Grünwald, N.J. 2009. Population genetic analysis infers migration pathways of Phytophthora ramorum in US nurseries. PLoS Pathog 5(9): e1000583.
Hansen, E.M., A. Kanaskie, S. Prospero, M. McWilliams, E.M. Goheen, N. Osterbauer, P. Reeser, and W. Sutton. 2008. Epidemiology of Phytophthora ramorum Oregon tanoak forests. Can. J. For. Res. 38:1133-1143. DOI: 10.1139/X07-217.
Kliejunas, John T. 2007. Sudden Oak Death and Phytophthora ramorum: A Summary of the Literature. Albany, California. Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture. http://www.suddenoakdeath.org/library/
Mascheretti, S.; Croucher, P.J.P.; Kozanitas, M.; Baker, L.; and Garbelotto, M. 2009. Genetic epidemiology of the Sudden Oak Death pathogen Phytophthora ramorum in California. Molecular Ecology 18: 4577–4590.
McPherson, B.A., Erbilgin, N., Wood, D.L., Svihra, P., Storer, A.J., and Standiford, R.B. 2008. Attraction of ambrosia and bark beetles to coast live oaks infected by Phytophthora ramorum. Agric. For. Entomol. 10, 315–321. doi: 10.1111/j.1461-9563.2008.00386.x
McPherson, B.A., Mori, S.R., Wood, D.L., Kelly, M., Storer, A.J., Svihra, P., et al. 2010. Responses of oaks and tanoaks to the sudden oak death pathogen after 8y of monitoring in two coastal California forests. For. Ecol. Manage. 259, 2248–2255. doi: 10.1016/j.foreco.2010.02.020
McPherson, B.A., S.R. Mori, S.O. Opiyo, A.O. Conrad, D.L. Wood, P. Bonello. 2014. Association between resistance to an introduced invasive pathogen and phenolic compounds that may serve as biomarkers in native oaks. Forest Ecology and Management 312 (2014) 154–160
NA2 in Oregon forests: California Oak Mortality Task Force Newsletter, June 2021 https://www.suddenoakdeath.org/library/newsletter-archive/
Rizzo, D.M. and M. Garbelotto. 2003. Sudden oak death: endangering California and Oregon forest ecosystems. . Ecol. Environ. 1(5): 197-204.
Tooley, P. and Browning, M. 2009. to Phytophthora ramorum Inoculum Production Potential of Some Common Eastern Forest Understory Plant Species. Plant Disease 93:3 Pages 249-256.
Tooley, P. and Kyde, K. 2007. of Some Eastern Forest Species to Phytophthora ramorum. Plant Disease , 435–438.
Werres, S.; Marwitz, R.; Man Int Veld, W.A.; Cock, A.W.; Bonants, P.J.M.; De Weerdt, M.; Themann, K.; Ilieva, E.; and Baayen, R.P. 2001. Phytophthora ramorum sp. nov., a new pathogen on Rhododendron and Viburnum. Mycol. Re. 105: 1155-1165.