Parke, J. L., and S. Lucas. 2008. Sudden oak death and ramorum blight. The Plant Health Instructor. DOI: 10.1094/PHI-I-2008-0227-01
Sudden oak death, ramorum leaf blight, ramorum shoot blight
More than 100 species of forest trees, native shrubs, herbaceous plants, and woody ornamental plants
Jennifer L. Parke and Sunny Lucas
Oregon State University, Corvallis, Oregon
Sudden oak death of tanoak (left) and ramorum blight of camellia (right) caused by Phytophthora ramorum.
Phytophthora ramorum is a recently emerged pathogen with a host range of more than 100 plant species. This fungus-like organism causes sudden oak death on certain members of the oak family, and has killed over 1 million trees in coastal forests in California. The pathogen also causes ramorum leaf blight or shoot blight on native plant species and horticultural nursery crops, and has plagued some nurseries in California, Oregon, Washington, British Columbia and in Europe.
Symptoms and Signs
Phytophthora ramorum causes two distinct sets of symptoms, depending on the host species. On certain members of the Fagaceae (oak family) such as tanoak (Lithocarpus densiflorus) and coast live oak (Quercus agrifolia), P. ramorum causes lethal bole (trunk) cankers resulting in the disease called sudden oak death (SOD). On other native plant species as well as many horticultural nursery crops, P. ramorum causes a foliar blight and shoot dieback. The disease on these hosts is referred to as ramorum leaf blight or ramorum shoot blight.
Sudden oak death
Bole and crown symptoms
P. ramorum infects the phloem and inner bark to cause bleeding cankers on susceptible members of the Fagaceae. The presence of these bleeding cankers is the most diagnostic symptom of SOD. Initially, individual spots exhibit a clear, reddish exudate on the main trunk of the host (Figure 1). As the disease progresses, this exudate may continue to seep through both cracked and intact bark (Figure 2). The affected area eventually stains a dark reddish-brown as the bleeding is diffused by rainfall (Figure 3). Removal of the outer bark reveals discolored areas (cankers) in the inner bark, often surrounded by a black line (Figures 4, 5). Cankers range from a few centimeters to 3 meters in length, developing most often in the lower part of the trunk but also as high as 25 meters from the ground. Cankers have only been found on mature coast live oak trees, but may appear on tanoak at any stage of development.
P. ramorum may also infect sapwood, restricting water transport in xylem vessels. The crown of infected plants often appears off-color before individual branches or the entire crown turns brown and dies (Figure 6). Infected stump sprouts may exhibit foliar necrosis, stem lesions, and wilted shoot tips known as “shepherd’s crooks” (Figure 7).
Foliar symptoms are not always observed on canker hosts, but tanoak leaves may exhibit mid-vein and petiole necrosis (Figure 8).
Ramorum leaf blight and ramorum shoot blight
Most hosts of P. ramorum exhibit symptoms chiefly on the foliage. On some hosts, lesions and vascular discoloration are associated with the stems. Plants susceptible to ramorum leaf blight or shoot blight (simply referred to henceforth as ramorum blight) include woody ornamental nursery stock as well as native herbs, shrubs, and trees other than the oak family hosts described above. On Rhododendron, necrotic lesions may appear anywhere on leaf surfaces (Figure 9) and are easily confused with lesions caused by other leaf-infecting species of Phytophthora. Leaf infection may occur through the petiole from infected stems, causing necrosis along the mid-vein (Figure 10). Foliar symptoms on other hosts vary, consisting of wedge-shaped or irregularly-shaped, darkened lesions that may appear watersoaked (Figure 11). Defoliation of affected camellia leaves is common (Figure 12). On California bay laurel (Umbellularia californica), necrosis is often confined to the leaf tip, with small yellow-brown spots scattered on other parts of the leaf (Figure 13). Conifers can also be hosts for P. ramorum, although disease incidence is usually limited to young trees beneath heavily infected bay laurel or tanoak (Figure 14). For a description of symptoms on various hosts, refer to the following sources: Davidson et al., 2003; Rizzo et al., 2002; Tjosvold et al., 2005; and The California Oak Mortality Task Force Website.
In greenhouse studies, P. ramorum infects the roots of several hosts, although it does not produce root rot symptoms typical of soilborne Phytophthora species. Root infection of nursery-propagated rhododendrons has been reported. It has been demonstrated that the pathogen can spread from the roots and up the stem to above-ground plant parts.
Although not detected on all hosts, sporangia (asexual fruiting structures) and hyphae of P. ramorum can be found on leaves, usually on the lower surface (Figure 15). Sporangia are only formed under very moist conditions. Chlamydospores (asexually produced survival structures) may also be found on or in infected leaf tissue of foliar hosts (Figure 16), or in the wood and bark of canker hosts.
Phytophthora ramorum is an oomycete (or water mold). No longer considered true fungi, these fungal-like organisms are now classified with brown algae in the Kingdom Stramenopila (or Straminipila, or Chromista). P. ramorum is a relatively new Phytophthora species, first isolated in Europe in 1993 but not described until 2001. P. ramorum is placed in the family Pythiaceae, order Peronosporales, and class Oomycetes; molecular phylogeny shows it to be most closely related to Phytophthora lateralis, a root pathogen of Port-Orford-cedar, and P. hibernalis (which causes brown rot of citrus fruit).
P. ramorum has a unique set of morphological traits that can be observed well on certain laboratory media (PARP medium, V8-juice agar, corn meal agar, or carrot agar). Vegetative growth consists of delicate, highly branched hyphae that grow in culture best at approximately 20 C (Figure 17). No mycelial growth is observed over 35 C. Asexual reproduction in the form of sporangia or chlamydospores is the most common form of reproduction for this oomycete. Sporangia can germinate directly or release motile zoospores. Large numbers of zoospores can be produced, ideally between the temperatures of 15-20 C. At 25 C, sporangia are more likely to germinate directly, by producing a germ tube. Sporangia are elongate, semi-papillate (have a short, rounded tip), and are sympodial (where each successive sporangium develops on a branch behind and to one side of the previous apex where growth has already ceased) (Figure 18). The sporangia of P. ramorum are produced on a short (< 5 µm) to nonexistent pedicel (stalk), are caducous (fall off easily), and measure 25-97 x 14-34 µm (length x width). P. ramorum sporangia are significantly more elongate than those of its closest relatives. This oomycete also forms many chlamydospores in vitro, which are hyaline (clear) when young, and turn golden brown in older cultures (Figure 19). Chlamydospores of P. ramorum are larger than chlamydospores of P. lateralis, averaging 40-80 µm, and are mostly terminal and rarely lateral, although some can be intercalary (develop within the hyphal strand).
P. ramorum is heterothallic, requiring opposite mating types designated as A1 and A2, for sexual reproduction. The A1 mating type is most commonly found in Europe and was first described there. The A2 mating type is most common in the U.S., although the A1 type has occasionally been observed in U.S. nurseries. Oospores (spores that result from sexual reproduction) are formed when an oogonium of one mating type is fertilized by the antheridium of the opposite mating type. Terminal oogonia are almost spherical and range in size from 24-40 µm in diameter (Figure 20). Antheridia are amphigynous (the oogonium grows through the antheridium) and also rounded. Oospores have only been observed under laboratory conditions and their role in disease development in nature is not known.
Disease Cycle and Epidemiology
|Disease cycle for P. ramorum in the forest (left; click to enlarge), and for P. ramorum in the nursery (right; click to enlarge).|
Because SOD and ramorum blight are diseases that have emerged recently, many details of the disease cycles are not yet understood. It appears that Phytophthora ramorum shares many characteristics of other aerially dispersed Phytophthora species. After infection of the host tissue, sporangia are produced and dispersed to new host material. There, the sporangia either germinate or release motile zoospores. A new infection event occurs, and the asexual cycle is repeated.
Ramorum blight is a polycyclic disease (has more than one disease cycle per growing season) on foliar hosts, producing many sporangia during wet conditions. Chlamydospores are produced in abundance by this pathogen and likely serve as a reservoir of inoculum during conditions unfavorable for disease development. SOD hosts are often considered "dead end" hosts because no sporangia are produced and mortality occurs as a result of canker formation or colonization of sapwood. However, sporulation has been observed on leaves and petioles of one canker host, tanoak. Sexual reproduction has not been observed in nature.
P. ramorum has a large host range that includes more than 100 species in over 40 genera. APHIS (the USDA Animal and Plant Health Inspection Service) maintains up-to-date lists of proven hosts and associated plants (those plants for which Koch’s postulates have not yet been confirmed) for P. ramorum. Not all species in a particular genus are susceptible, and within a given species a gradient of susceptibility among individuals is often evident. The factors that cause these differing responses by closely related species are not known. P. ramorum has been found in the nursery, the forest, and the urban-wildland interface. In 2006, P. ramorum was detected in 62 nursery-related sites in 11 states. Outside of nurseries, in 2007, ramorum blight affected coastal mixed-evergreen forests in 14 counties in California and in part of one county in southwest Oregon (Figure 21). It occurs discontinuously, not necessarily affecting all potential hosts. P. ramorum is believed to be exotic to both North America and Europe.
Genotyping of P. ramorum isolates shows that there are three clonal lineages: EU1, NA1 and NA2 (Table 1). These distinct genetic lineages suggest that strains were likely introduced separately to Europe and North America from P. ramorum’s unknown geographic origin. The finding of both EU1 (mating type A1) and NA1 (mating type A2) isolates from the same nursery in California in 2007 introduces the possibility that sexual reproduction could occur as it does in its place of origin. This underscores the need to prevent movement of nursery stock infected with P. ramorum.
Table 1. The three clonal lineages of Phytophthora ramorum in relation to distribution and mating type.
In Europe, ramorum blight was first observed on rhododendron and viburnum in the early 1990s and by 2007 had spread throughout nurseries and retail centers in 16 countries. In addition, the pathogen has been detected in gardens, parks, and woodlands in eight countries. In a few gardens and parklands in the U.K. and the Netherlands, beech and oak trees have begun to show symptoms of disease. In most cases, the trees are adjacent to infected rhododendrons.
As with other aerial Phytophthoras, P. ramorum is likely transmitted by rain splash, air currents, and wind-driven rain, but the specific details of dispersal and infection are not fully known. Sporangia are believed to be moved by air currents following wet weather. They likely initiate leaf and twig infections high in the forest canopy. Following rain or fog, more sporangia are produced, which can be blown or splashed to other leaves. They may also run down the bole with rainwater, initiating cankers on susceptible hosts. Infections often spread from taller trees to understory trees and shrubs beneath them. Root infection has been observed on young tanoak seedlings in heavily infested forests, but the epidemiological significance of this is not known, since abundant aerial inoculum was also present at these sites. There is a high risk of propagule transmission by humans who move infested plant material, logs, and soil. In the forest setting, viable propagules can get lodged on the shoes of hikers or on bicycle tires, but it is not known if these soilborne propagules can initiate disease. P. ramorum can be recovered from streams in infested areas, but it does not appear that this has led to new infections in the forest. While these and other potential bird, mammal, and insect vectors have not been ruled out, the pattern of disease occurrence in the forest is most consistent with windborne dispersal of inoculum.
In the forest setting, P. ramorum follows a classic dispersal gradient. Most inoculum remains within 5-10 m of the host, and the number of propagules decreases with distance from site of formation. Yet, it is possible that a few propagules are dispersed long distances. Caducous sporangia carried above the canopy during a storm event might initiate an infection far from their origin. This is a likely scenario of what occurred in Curry County, Oregon, as this site is 400 miles from the nearest known infested forest site.
P. ramorum does not sporulate on all hosts. Reproductive propagules have not been recovered from at least one of the species most devastated by SOD, coast live oak. However, sporangia are produced readily on the foliage of California bay laurel, which is commonly found in association with coast live oak and tanoak in infested forests in California. Ramorum blight is not lethal on bay laurel. It is thought that sporangia and zoospores produced on bay laurel can readily infect coast live oak and tanoak in the forest. The ecology of chlamydospores is poorly understood. Chlamydospores are produced in or on leaves of some hosts. When infested leaves fall to the ground or chlamydospores are shed, it is hypothesized that chlamydospores may lie dormant during the dry summer, then eventually germinate and produce more sporangia when the winter rains arrive, initiating new infections.
In horticultural nurseries, infections have been found up to 0.5 m from the closest infected plant, but infections due to long distance wind dispersal have not yet been noted. Irrigation water can be an inoculum source for nurseries using contaminated recycled irrigation water or water from infested streams. Rhododendrons and some other nursery plants can become infected through their roots if inoculum is present in the potting mix.
Long-distance dispersal of P. ramorum is facilitated by shipments of infected nursery plants across the country. For example, in 2004, a large wholesale nursery in southern California shipped 1.6 million camellias throughout the U.S. (Figure 22, 23). The nursery was later found to be infested with P. ramorum (Figure 24). Although APHIS checked each of the nurseries that had received plants and destroyed the plants that were infected, many had already been sold. Despite fears that these infected camellias might spread the disease to surrounding forests, there is no evidence yet that P. ramorum has become established in forests outside of California and Oregon. P. ramorum has since been detected in several other west coast nurseries (see Diagnosis and Monitoring), which is why plant material must be certified as free of P. ramorum before host plants are shipped from these west coast states.
Because Phytophthora ramorum is a quarantined pathogen that affects plants in both forests and nurseries, disease management is complex. It requires cooperation among federal, state, and county agencies as well as private industry to protect natural resources while not unduly limiting nursery commerce. The difficulty of disease management is compounded by our incomplete knowledge of the pathogen’s biology. As more is discovered about the pathogen, more effective control strategies can be developed.
Diagnosis and Monitoring
It is important to quickly and accurately identify symptoms caused by P. ramorum in the nursery, forest, or landscape. Since symptoms vary by host and are not diagnostic, best results have been achieved by combining polymerase chain reaction (PCR) based assays with the more traditional method of isolating the pathogen from symptomatic tissue on the selective laboratory medium PARP. Enzyme-linked immunosorbent assay (ELISA) kits designed for field detection of Phytophthora species can be a useful screening tool.
Nursery growers must systematically inspect plants and propagative material to prevent introduction of the pathogen to existing stock. In the field, monitoring must continue in both infested and non-infested areas. The use of aerial and ground surveys, stream baiting in high-risk watersheds, and monitoring by trained members of the community must all be used in concert. Effective education and communication are essential for preventing the spread of P. ramorum. Programs and training sessions have been established for nursery employees, Master Gardeners, Extension personnel, arborists, landscapers, utility workers, recreationalists, and homeowners. Web-based resources include photos of symptoms on hosts, questionnaires to help determine the need for submitting a sample, and instructions for collecting a sample.
APHIS and the U.S. Forest Service have conducted several national surveys to estimate the geographic distribution of P. ramorum in nurseries and forests. At the end of 2004, the pathogen had been detected on nursery stock in 21 states and British Columbia. In 2005, 99 nursery sites in 7 states were found to be positive for the pathogen. Despite these findings, national surveys of forest lands and nursery perimeters have not detected the pathogen outside of California and southwest Oregon.
The most effective way to prevent P. ramorum from becoming established is to keep it out of non-infested areas. Preventing human-facilitated spread of the disease is critical. Evidence from Europe suggests that infected ornamental plants can spread Phytophthora species to the forest. Therefore, P. ramorum is a quarantined pathogen, and international and interstate movement of hosts and associated hosts in California, Oregon, and Washington is federally regulated. Much of this entails nursery inspections and testing in quarantined areas. Nursery certification programs have been established to ensure that nurseries are in compliance with preventive protocol. Specific “best management practices” (BMPs) are recommended to prevent establishment and further spread of the disease. BMPs include monitoring all known hosts for symptom development, inspecting all incoming plant stock for symptoms of disease, and confirming that all incoming stock originates from a shipping nursery that has a USDA SOD compliance agreement or has been certified pathogen-free. For a list of BMPs, refer to the California Oak Mortality Task Force Website. Movement of infected logs (including firewood), infested soil, and litter outside infested counties are all strictly prohibited. Even within quarantined counties, one should not move infested materials. To prevent further spread through California forests, signage and devices for cleaning shoes and bicycles are being installed along trailheads in infested areas.
As part of BMP strategies to avoid introduction of P. ramorum, growers are encouraged to segregate the two highest-risk genera, rhododendron and camellia, from the rest of their nursery stock. They are also asked to avoid conditions that are conducive to the development of Phytophthora diseases by improving drainage and irrigating in such a way as to minimize the period of leaf wetness. Nurseries in infested areas should also remove potential native hosts, especially bay laurel trees, from their property.
Eradication may be a viable option if the disease is caught relatively early after introduction. For example, the state of Oregon established a proactive eradication program in 2001 in an attempt to control P. ramorum in Curry County in the southwest corner of the state. All hosts within 100 feet (approximately 30.5 m) of symptomatic hosts are cut, piled, and burned. Cut stumps are also treated with herbicides to reduce sprouting. Sites are then monitored for two years to confirm that the eradication process has been successful. Although the pathogen has still spread to new sites in Curry County, the infection rate appears to be less than in similar forests in northern California where eradication programs were not implemented. Approximately 579 ha (1,430 acres) in Curry County have been treated to date (Figure 25). This type of eradication program is not feasible if the disease is already widespread, or if infected vegetation is intermingled with residences.
In all nurseries, infected plants must be destroyed as part of the eradication program. If infected plants are found in a particular nursery, corresponding nurseries receiving or sending these plant materials are also inspected as part of the APHIS protocol. Infected material at these sites, as well as plants within a buffer zone of 2 m, are then destroyed (Figure 26). Healthy-appearing plants within 10 m of infected plants are held for observation for a period of time to see if symptoms develop.
On a smaller scale, eradication of inoculum from soil or contaminated containers can be achieved through treatment with aerated steam (65°C for 30 min) or by treatment with soil fumigants. Two facilities in California are also certified to “hot compost” green waste that is infested with P. ramorum.
Protection consists of treating a healthy plant before it comes in contact with the pathogen. An important aspect of fungicide application in nurseries is to ensure that treated plants are not already infected with the pathogen. Most fungicides do not kill Phytophthora; rather they temporarily suppress symptom development, delaying detection until after the plants are shipped. Therefore, if fungicides are used, they should only be used to prevent infection and should not be applied to potentially infected plants. Several chemicals, including mefenoxam, dimethomorph, pyraclostrobin, and fenamidone, may protect nursery hosts such as rhododendron from infection. Permitted uses vary for different hosts and in different states and countries. While fungicide resistance has not yet been reported in the U.S., resistance of P. ramorum to metalaxyl has been reported in Europe. There is still more work to be done to determine dosages, application timing, and hosts to be treated. Preventive treatment of forest trees with fungicides is not economically feasible, nor is it permitted on public lands. Individual high-value trees on private property may be treated with phosphite fungicides by direct injection or by mixing them with organosilicate surfactant-penetrants applied to the bark. Both methods have been shown to reduce disease development on canker hosts, and these chemicals are registered in California.
There is considerable variation in host resistance among genera and species of susceptible plants. For example, significant variation in susceptibility among individual oaks, tanoaks, and bay laurel has been observed. Variation in virulence has also been seen among U.S. isolates of P. ramorum. So far host specificity has not been found for particular isolates. Of the many plants that have been tested for susceptibility to P. ramorum in laboratory studies, very few species appear to be immune.
Phytophthora ramorum is a recently emerged pathogen, thus the ultimate significance of SOD and ramorum blight is still unknown. Without a thorough understanding of the pathogen’s biology, it is still too early to predict the magnitude and future impact of this disease. The climate in coastal areas of Washington, Oregon, and California as well as large areas of the southeastern U.S. is considered suitable for P. ramorum (Figure 27). The fear is that this disease could spread by infested nursery plants to the eastern U.S. where susceptible oak-hickory, oak-pine, and lowland oak forests account for 67.8 million ha (167.5 million acres), or 46% of the total area classified as timberland. In greenhouse tests, several important east coast tree species were found to be highly susceptible to the disease.
Other exotic Phytophthora species have led to extensive tree mortality and negative ecological impacts in Australia, Europe, and North America. The desire to prevent an outbreak as devastating as historical epidemics like Dutch elm disease and chestnut blight has led to cooperative efforts between governmental officials, business owners, academia, and the public.
SOD has already changed the landscape of coastal California forests, where it is estimated that over 1 million trees have been killed in the last 10 years. The disease is lethal to the multiple oak species and tanoaks that make up a substantial part of several mixed-evergreen forest types in California, thus it will greatly alter the composition of these forests. Wildlife habitats will be affected. Since dead trees create an enormous fire hazard, fire management strategies will have to be considered in areas heavily hit by the disease. The ecological implications of this epidemic are as yet unknown.
P. ramorum has also placed a financial burden on the nursery industry on the west coast. Nursery sales make up a substantial portion of the agricultural economy for all three states currently under quarantine, and ramorum blight affects some of the most profitable and popular nursery crops for interstate commerce. Crop destruction, loss of sales, new disease management practices, inspections, training, testing, and increased documentation have required a huge commitment of both time and money. P. ramorum has forced many changes in the nursery industry nationally, highlighting the need for more effective methods for dealing with quarantine pests and pathogens.
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