- Phytophthora ramorum was introduced to natural systems or nurseries in 32 countries as of July 2021 (Hieno et al. 2022)
- It infests plants in more than 70 genera; some are killed, others survive; some hosts support spread of the infection (see detailed descriptions below).
- In North America, host species and genera include ashes, California bay laurel (Oregon myrtle), camellias, hemlock, huckleberries, larch, lilacs, Pacific madrone, magnolias, maples, mountain laurel, oaks, rhododendrons, and viburnums.
- Phytophthora ramorum was probably introduced to North America on infected imported plants in the late 1980’s or early 1990’s. It is likely there were several introductions over the years.
- In North America, three of four known genetic strains are now established in wildland forests – three in Oregon, two in California.
- P. ramorum probably originates in the mountains of Southeast Asia, specifically from Vietnam to Japan (Jung et al. 2020). This region is also the probable source of the Euwallacea complex of ambrosia beetles transporting pathogenic Fusarium fungi.
Sudden Oak Death (SOD) first came to attention in the mid-1990s, when a large number of oaks and tanoaks (Notholithocarpus densiflorus) began dying 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 subsequently named Phytophthora ramorum. Since 2004, SOD has spread to 16 coastal California counties, from Monterey north to Del Norte, as well as in Curry County, Oregon. 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: 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 (Kozanitas et al. 2022). An estimated 91.4 million infected California bay laurel trees were present in the state in 2014.
These estimates are considered conservative because they are based only on trees that were confirmed as infected by direct, cultural isolation before 2014. The infection continues to intensify when weather patterns are favorable; thus, the wet winters of 2016-2017 led to a large increase in tanoak mortality in California counties reaching from Mendocino south to Monterey (September 2018 COMTF) By 2021 new infections were greatly reduced in California as a result of the drought (February 2022 COMTF).
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 the affected host species are the dominant hardwoods over large areas, growing in nearly pure stands. Tanoak is the principal hardwood /mast-bearing species in mixed tanoak-redwood forests. P. ramorum is now known to infect nearly all of the major trees species in California’s infested counties. Death of SOD-infested trees can be accelerated by attacks by bark and ambrosia beetles (McPherson et al., 2008; 2010). Introduction of a new ambrosia beetle from Europe, Mediterranean oak borer (Xyleborus monographus) might exacerbate this situation.
The disease can even affect 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. 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.
At least five global migrations of Phytophthora ramorum have occurred. Of the four clonal lineages that have been identified, three – NA1, NA2, and EU1 – have been imported into North America and two lineages – EU1 and EU2 – into Europe. The most likely form of transport has been the ornamental plant trade. It is believed that the US and Canada received the EU1 lineage unknowingly through importation from Europe. In 2021, scientists discovered that the North American and European lineages established in Oregon forests were hybridizing. These hybrids are viable; they can infect a host and produce spores for long-term survival and propagation (Hamelin et al. 2022).
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 assess pathogen viability in the eastern US, it is necessary to determine 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, presence of the disease was confirmed in 16 counties as of early 2022, reaching from Del Norte in the north to southern Monterrey County in the South. 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 (February 2021 COMTF).
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. When that proved impossible, authorities adopted a slow-the-spread strategy emphasizing early detection and treatment of outbreaks on the edge of the infestation in 2010. Periodic wet periods have led to expansion and intensification of the disease in Curry County, leading to expansion of the quarantined area. By 2021, outbreaks were detected nearly 30 miles north of the Generally Infested Area. Control of this epidemic has cost more than $32 million by 2020 (LeBoldus et al. 2022). The Oregon state legislature appropriated another $1.7 million in 2021 (COMTF Feb 22). Between September 2021 and June 2022, Oregon Department of Forestry (ODF) spent $624,000 on SOD treatment work in the Port Orford area. Experience indicates that it will cost $1,247,400 to treat the remaining infested acreage, but available funding is only $1,197,000. ODF does not have the treatment budget or staff time to complete treatments within the SOD quarantine zone at this point given the priority placed on the Port Orford treatment area (COMTF June 22).
At least three invasions of three separate variants (clonal lineages) have occurred in Oregon. The original strain was NA1. When the EU1 strain was detected in 2015, authorities assigned the highest priority to eradicating those outbreaks. Detection of the NA2 strain occurred in 2021 which is thought to be four years after actual introduction. This forced authorities to focus on the highly virulent NA2 strain and postpone efforts addressing the others (LeBoldus et al. 2022). Federal agencies have 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, although Oregon’s management efforts have reduced inoculum and limited the spread of both the original NA1 and EU1 strains of the pathogen (Daniels et al. 2022). 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).
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).
Noting that markets for carbon credits are important components of policies addressing climate change, Badgley and colleagues (2022) raise alarm about the probable impact of introduced pests. They found that the potential carbon losses associated with death of a single species, tanoak, caused by a single forest disease – SOD – could use up all the credits set aside in the California program to absorb disease and insect risks. Since U.S. forests are expected to experience increased mortality due to additional pest introductions, they argue that California’s credit market is unlikely to be able to guarantee the environmental integrity of California’s forest offsets program for 100 years.
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 steep learning curve associated with discovery of the pathogen 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 southern 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. Earlier federal regulations, adopted in 2002, had addressed only the 14 infested California counties and the infested area of Curry County, Oregon.
APHIS’ broader regulations substantially reduced but did not eliminate the presence of P. ramorum on nursery stock. There have been periodic major episodes of SOD spread in the nursery trade. Between 2003 and 2011, 464 nurseries in 27 states 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, it was 16 nurseries. In 2019, nurseries in 18 states received plants possibly infected by the pathogen; positive plants were confirmed in seven states (August 2019 COMTF).
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. It wasn’t until 2014 that APHIS began requiring nurseries that tested positive for P. ramorum to adopt APHIS-approved integrated management programs to address all the identified high-risk actions (Confirmed Nursery Protocol). The agency also began testing water, soil, and other potentially-infested articles in the nursery, not just potentially diseased plants.
The number of nurseries in California and Oregon detected as having SOD-infected plants continues to decline. In 2021 seven such nurseries were detected in the two states. In 2022, no California nurseries were positive for the pathogen, while about a half-dozen nurseries continued to be infested in Oregon. As in past years, several nursery detections result from trace-forward or trace-back investigations rather than mandated periodic inspections. Nurseries in Washington and British Columbia have also been involved in investigations occasionally – although Canadian authorities commonly reply that they can find no sign of infection.
With these continuing problems, APHIS has re-evaluated its program several times. In May 2019, immediately before the nursery spread event mentioned above, APHIS revised its regulation to incorporate practices previously adopted through Federal Orders. APHIS’ goal was to reduce the regulatory burden on nurseries in areas that are regulated for P. ramorum, while still ensuring that nurseries that may pose a risk of disseminating P. ramorum through the interstate movement of regulated nursery stock are subject to measures that address this risk. APHIS hoped to focus its own and state agencies’ efforts on the nurseries that present a significant risk of spreading the pathogen and away from those nurseries that pose a negligible risk. The revised regulations did not change then-operational requirements, but rather codified protocols in place since 2014. The principal components were as follows:
- Nurseries located in the P. ramorum quarantine zone in California and Oregon must undergo annual inspection, sampling, and testing.
- Nurseries located anywhere that ship P. ramorum host plants interstate are subject to regulation if P. ramorum has been detected less than three years previously.
- Inspections include sampling and testing of potting soil, water, pots, and other potential sources of P. ramorum inoculum rather than only the plants themselves.
- Nurseries under regulation – wherever located – must enter and comply with the terms of APHIS’ compliance agreement in order to ship P. ramorum host plants interstate.
- Nurseries under regulation must submit plants that are P. ramorum hosts to inspection before shipping them interstate.
In 2022, the new Deputy Administrator of APHIS reported that it was again reviewing the program and would shortly share its new procedures for review by the states. He said that the conclusion was that unless the environment changes, P. ramorum is unlikely to threaten forests outside California and Oregon (presentation to National Plant Board annual meeting August 2022).
A major concern is the continuing presence of the pathogen in nurseries that have carried out the USDA APHIS Confirmed Nursery Protocol. 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 such case occurred in Washington in 2009, when salal (Gaultheria shallon) plants apparently became infected by water flowing from an infested nursery. The salal was been removed, and the area paved.
USDA Forest Service testing of streams (starting in 2006) has surveyed more than 320 watersheds. As of 2013, this survey had identified seven streams in Washington State and 11 streams in the Southeast as bearing P. ramorum. Most of the Southeastern streams have remained positive. Only one example, however, has detected associated infected plants: in Mississippi early in the program. Oregon and California operate their own, more extensive, stream survey programs. While California detects the pathogen in streams downstream from known and unknown infected forest areas, Oregon has never found P. ramorum in streams outside the Curry County outbreak area.
Before the pathogen was formally named, it was found in Europe 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. 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, which helps to minimize the risk of further disease development or pathogen spread. Research also continued 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. As part of this project, Green et al. (2021) identified 63 species of Phytophthora in UK nurseries. Several of the species are considered pathogenic; several were potential new records for the U.K.
Also in 2009, P. ramorum was found in mature plantations of Japanese larch (Larix kaempferi), a species widely planted in the British Isles. 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 – previously the most common infectious host.
In 2019, the infestation expanded and intensified in western Scotland, England, and Wales (February 2021 COMTF). P. ramorum is also present in Ireland; the Republic has only the EU1 strain; Northern Ireland has both EU1 & EU2 (O’Hanlon et al. 2021).
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 September).
For more information on P. ramorum and Sudden Oak Death, go to the California Oak Mortality Task Force website at www.suddenoakdeath.org.
Other Phytophthora diseases
Forest diseases caused by an ever-growing number of Phytophtora species other than P. ramorum have been detected at an escalating rate since the late 1960’s (Jung et al. 2020). These include:
In North America:
- P. pseudosyringae on red alder (Alnus rubra) and white alder (A. rhombifolia)
- P. kernoviae on many tree and shrub species, including European beech (Fagus sylvatica) and rhododendron (Rhodendron ponticum)
- P. lateralis on cedars (including but not limited to Chamycaeparis lawsonii; also Cupressus and Thuja), and other conifers
- P. austrocedri on common juniper (Juniperus communis)
- several Phytophthora on alder (Alnus)
- P. pluvialis on western hemlock (Tsuga heterophylla)
The situation on the European continent was even worse. As of 2015, 91% of 732 European nurseries producing larger trees for forest and landscape uses were infected by one or more Phytophthora species (Jung et al. 2015). A total of 49 Phytophthora species were detected in these nurseries. Fifty-six Phytophthora taxa were detected in forest and landscape plantings. The total number of distinct taxonomic entities was 68.
In New Zealand, P. agathidicida is attacking the huge endemic tree, kauri (Agathis australis).
Fixing phytosanitary system
A growing number of scientists have noted that the international phytosanitary system has not been successful in preventing introductions of pathogens via the international nursery trade (Brasier 2008; Liebhold el. al. 2012; Santini et al. 2012; Roy et al. 2014; Eschen et al. 2015; Jung et al. 2016; Meurisse et al. 2019). O’Hanlon et al. (2021) specify the failures recognized by most of these experts for more than a decade: (i) visual inspections can miss asymptomatic infections, (ii) limited resources mean only a small proportion of commodities can be inspected, (iii) allowing the use of fungicides masks disease symptoms on plants, (iv) list-based regulations don’t address undescribed organisms and (v) countries vary in how aggressively they carry out the required phytosanitary procedures. They conclude that “Until these issues are addressed it is likely further increases in the numbers of non-native pests and pathogens of trees will increase.”
There are some promising developments in the form of improved detection methods. Espindola et al. (2022) describe advancements in high-throughput sequencing (HTS) technology, which allows the detection of pathogens without the need for isolation or template amplification. They say that plant regulatory agencies worldwide are adopting HTS. Hieno et al. (2022) describe a different technique, loop-mediated isothermal amplification (LAMP).
An earlier version of this write-up benefited from significant input from Katie (Palmieri) Harrell, then with the California Oak Mortality Task Force.
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