Since 1995, mortality of at least three native California oak species has reached epidemic levels (McPherson et al. 2000). The seemingly rapid decline of these trees is triggered by a new species of Phytophthora (a funguslike organism). Named sudden oak death (SOD), or oak mortality syndrome, this disease has never before been observed in California. SOD has received substantial attention by the media and the public because oaks not only represent a major component of many California forest ecosystems, they are also important both in urban landscapes and at the urban/rural interface. Tanoak, coast live oak and black oak trees are distributed along 1,500 miles of the California and Oregon coast. Researchers, land managers and policy-makers are using adaptive management to direct their efforts, but are faced with the challenge of formulating control guidelines based on a limited and still evolving understanding of the disease.

This article summarizes the current knowledge about sudden oak death and refers to some of the ongoing experiments designed to provide insights into its possible causes. Finally, we address potential options for control. Because this work is in progress, most of this information should be treated as preliminary. Often we rely on references to similar but not identical problems in other systems. The information presented here has been condensed from the work of many researchers actively involved in the study of SOD. Among them are Susan Frankel, Thomas Gordon, Kent Julin, Maggi Kelly, Steve Koike, Brice McPherson, Nicole Palkowsky, Garey Slaughter, Andrew Storer, Ted Swiecki, Steve Tjosvold, Ellie Rilla, Rick Standiford and David Wood.

What is sudden oak death?

Sudden oak death (Svihra 1999) is known to affect three tree species: California tanoak (Lithocarpus densiflora), coast live oak (Quercus agrifolia) and California black oak (Q. kelloggii). We have also isolated the pathogen from rhododendrons. Although SOD has been reported only in central and northern coastal California (fig. 1), the natural range of tanoaks and black oaks extends well into the interior ranges of California and into Oregon. Coast live oak is found throughout Southern California and into Baja California, Mexico. In addition, the presence of SOD on a commercial ornamental plant (rhododendron) raises the possiblity that it may already have been disseminated more widely than we know. Its presence in ornamental plants could be temporarily masked by the use of fungicides.

We still do not understand patterns and mechanisms of dispersal of this new disease. Therefore it is not known whether SOD will expand throughout the range of its hosts, or whether its distribution will be limited by factors such as climate, presence of competing organisms and predators, or absence of potential vectors. The disease is currently patchy in its regional distribution, but can affect 40% to 80% of trees in any given stand. Such high levels of oak mortality are unprecedented in California, and suggest the emergence of a new disease.

Trees affected by SOD display a range of symptoms depending on stage of infection, tree species and the time of year. Wilting of apical shoots is a common initial symptom of infected tanoaks. Sparse pale-green foliage is observed in coast live oaks in an advanced stage of the syndrome. Mature trees of all three host species affected by SOD display bleeding and sunken cankers on the bole, or trunk. These cankers are more frequent on the lower part of the trunk, but they can be found up to 30 feet (10 meters) from the base of the tree. Cankers seep a dark brown or amber-colored sap. Such seeping is the most dependable symptom of a tree affected by SOD. Intensity of seeping varies among different trees and may fluctuate on the same tree, perhaps depending on the time of year or stage of canker development. For instance, seeping tends to decrease during dry periods and in older cankers. In smaller tanoaks, no seeping may be associated with the cankers, which appear water-soaked and may be scattered on stems.

In later stages of SOD, coal-black dome-shaped fruiting bodies of the fungus Hypoxylon thuorsianum invariably develop. At first the black fungal domes appear near and above the canker areas and then over large portions of the bole. Beetles (Coleoptera: Scolytidae) are also consistently found on trees in later stages of SOD. The western oak bark beetle (Pseudopityophthorus pubipennis) and ambrosia beetle (Monarthrum spp.) feed respectively on the bark (phloem) and sapwood of host trees. Their feeding activity results in barely visible tunnels on the tree bark and in the production of finely ground frass (chewed phloem or sapwood) that accumulates, often in large amounts, on the tree bark. We believe that in spite of the strong association between Hypoxylon and/or beetles and tree mortality, these organisms should be considered as secondary. Such organisms are present on declining oaks worldwide, no matter what the cause of the decline.

We have isolated an oomycete fungus belonging to the genus Phytophthora from many trees with SOD symptoms. Many oomycetes are aggressive plant pathogens, including the pathogen responsible for the infamous Irish potato blight of the 19th century. We succeeded in isolating Phytophthora from SOD-related seeping cankers at the root crown to over 10 feet (3 meters) above the ground. Seeping, a likely host defense response, may provide the fungus with a potential route of dispersal for its infectious propagules. These propagules, called sporangia, have been found in the sap oozing from cankers during wet and cool periods. From there, the sporangia may either be splashed onto other trees or possibly transported by animals. Infection on a new host begins in the phloem, progresses to the cambium and eventually reaches the xylem. The phloem is often a bright red with numerous thin black lines that delimit the canker. Infection and discoloration are always more extensive in phloem tissues than in xylem. Black discoloration can extend up to 3/4 inch (2 cm) into the xylem below the bleeding canker. Discoloration in the phloem and xylem may extend up to 20 inches (50 cm) in all directions from the point of bleeding. Phytophthora is typically isolated from the margins of these discolored areas, although it can often be isolated from older portions of the cankers. Cankers on smaller tanoaks are not as distinct, and zone lines are not always apparent in either phloem or xylem.

Elevated oak mortality caused by other species in the genus Phytophthora has been reported from other regions of the world (Brasier et al. 1993, Jung et al. 1999, Tainter et al. 2000). For decades, a few Phytophthora species (P. cinnamomi, P. citricola and P. cactorum) have been known to be present on oaks in California. However, the newly isolated Phytophthora does not match the morphology of any of the known described species (Erwin and Ribeiro 1996), and is still unnamed. In this paper, we refer to this new species as SOD Phytophthora. DNA analysis also indicates that this is a new undescribed species, whose only close relative is another Phytophthora species (P. lateralis), which is present only in California, Oregon and Washington. This related pathogen, considered by many to be an exotic species, is extremely virulent on Port Orford cedar (Chamaecyparis lawsoniana) in the Pacific Northwest. Although the two species of oomycetes are morphologically different and attack different tree species, they share the same requirement for cool climates, they do not tolerate temperatures over 95°F (35°C). Both species also produce similar chlamydospores, thick-walled propagules that ensure survival of the pathogen in harsher climatic conditions or unfavorable environments.

The role played by chlamydospores and most of the biology of the SOD Phytophthora is still unknown. Phytophthora lateralis and many other Phytophthora species are dispersed through the movement of soil and water contaminated by chlamydospores. This mode of dispersal needs to be verified for the SOD species. Whether and for how long the pathogen can survive in dead wood is also still undetermined. Although our observations indicate that the pathogen can infect trees by penetrating directly through the unbroken bark, the importance of wounds and of potential vectors needs to be investigated.

One feature that appears to differentiate the SOD Phytophthora from other forest Phytophthora species is the presence of an aerial component. This component, inferred from the presence of aerial cankers, can be determined by the cauducous nature of the sporangia. This feature may allow these infectious propagules to detach from the fungal colony and become airborne. A significant aerial component in the disease cycle may also explain the lack of a strict association between patterns of disease spread and the presence of water. Such association is normally observed for nonaerial Phytophthoras.

Understanding whether the SOD pathogen may be (a) introduced; (b) a new taxonomic entity obtained by hybridization between P. lateralis and another Phytophthora species; or (c) a native pathogen may help in predicting the final impact that SOD is going to have on oak ecosystems. Non-native or new diseases often find plant hosts ill-equipped to defend themselves, and the result can be host decimation. Native diseases may cause epidemics due to increased host predisposition, bu they rarely wipe out entire host species.

We also do not know whether or not this pathogen completes its sexual cycle. In general, pathogens that are capable of completing the sexual cycle are more successful both in adapting to new environments and in developing resistance to compounds used for chemical treatments.

Probable primary causal agent

Although SOD may ultimately be the result of a complex scenario in which several pathogens, pests and abiotic factors interact with one another, the new Phytophthora seems to be found on all trees affected by SOD. This was evidenced by direct isolations of the pathogen from the hosts or by the presence of typical sunken cankers and seeping. This strong association suggests that this organism is the primary causal agent of the syndrome. Inoculations of seedlings, saplings and adult trees have been performed to confirm its pathogenicity. Preliminary results from all three experiments indicate that this oomcycete is capable of causing disease symptoms on inoculated hosts comparable to those in naturally infected plants.

Although there is also a striking correlation between SOD and both Hypoxylon and beetle attacks, we believe that these and other organisms may play a secondary role. Fungi in the genus Hypoxylon are normally endophytically present and inactive in the host, until mechanical damage, insects or diseases create the right environmental conditions for their growth. Twig or stem cankers caused by fungi other than Phytophthora (for example, Botryosphaeria spp.) are also often abundant in areas affected by SOD. These are considered as secondary or opportunistic organisms that thrive on trees weakened by other factors. The correlation between insect attacks and dead trees is striking, and much remains to be understood about the role played by insects. Although it is undisputed that insects speed the death rate of trees, it is unclear whether they are significant vectors for the pathogen and necessary to kill trees.

Although vectoring by beetles or other insects cannot be excluded at this point, our observations indicate that many cankers are initiated without any sign of beetle activity. There are also many cases in which small trees, although unsuitable for colonization by such insects, are infected by the new Phytophthora species and die, again suggesting a secondary role played by insects in SOD.

Marin County field study

In March 2000, 67 coast live oaks were sprayed with the insecticide Astro (36.8% active ingredient permethrin), according to label directions, on the lower 12 feet (4 meters) of tree boles on a Marin County ranch heavily affected by SOD. Only live trees (both healthy and symptomatic) were treated and marked. Trees with extremely thin crowns and abundant signs of beetle activity were regarded as dead and therefore excluded from treatments.

In July 2000, we returned to the site and performed a comparative evaluation of the 67 treated trees (Astro group) versus 67 untreated trees (non-Astro group) in an adjacent stand. None of the trees in the Astro group displayed signs of beetle activity on the treated portions of the boles, while 11 (16%) of the non-Astro trees showed symptoms of beetle attacks (fig. 2).

The two groups were well suited for a comparison:

The overall mortality at the study site (that is, including all 134 trees from the Astro and the non-Astro groups) was approximately 13% (17 individual trees). The number of seeping cankers showed that the levels of infection were not different between Astro-treated and nontreated groups (fig. 2). A total of 9 trees (13%) in the Astro group were dead, despite the notable absence of bark beetles and ambrosia beetles in the treated portion of the trunk. All of the dead trees in the Astro group were mature, and had been killed without the presence of bark beetles. However, all dead trees displayed Phytophthora-caused bleeding cankers, providing strong support of Phytophthora as the primary causal agent of SOD. Furthermore, levels of mortality were not significantly different between the two groups (fig. 2), providing further evidence that insects were not the primary cause of SOD-linked mortality. Finally, all trees in the non-Astro group attacked by beetles (11) also had bleeding cankers, but 22 other trees displayed bleeding cankers without signs of beetle activity. This result reinforces the observation that cankers precede beetle attacks, and that fungal colonization is a factor predisposing trees to attacks by bark and ambrosia beetles.

Both inoculation tests and this beetle-exclusion study point to Phytophthora as the most likely primary agent of SOD in California. Nevertheless, secondary agents including insects and other pathogens are bound to play a significant role. For instance, it has been reported that insecticide applications delay tree mortality for several months (Svihra 2000). This information clearly indicates that insect attacks strongly contribute to accelerated tree death. Our current challenge is to understand the basic biology of the SOD Phytophthora in relation to the plant hosts and to the other agents involved in SOD. An effective control strategy will be feasible only when the sequence of possible interactions among all damaging agents is better understood.

Integrated management approach

We have just begun to unravel some of the dynamics of SOD, and research and outreach professionals are hard pressed to provide control strategies that may lead to disease containment or remission. The three main issues of disease management pertain to our ability to (a) prevent further spread of the disease; (b) contain disease intensity where it is already present; and (c) identify treatments capable of arresting or remitting disease development on infected trees.

Even though cures have rarely been developed for tree diseases, it is not unrealistic to envision a combination of cultural and chemical treatments that may prove effective against the spread of SOD. The extent of control depends largely on the type of strategies available and on their costs, both economic and environmental. The more targeted and less costly the approach, the broader its application. It is also important to keep in mind that landscape trees may display symptoms identical to SOD, but be infected by Phytophthora species other than the SOD Phytophthora. A precise diagnosis is therefore essential, because other Phytophthora-caused diseases require different control approaches. Furthermore, all SOD control strategies must be accompanied by general practices aimed at enhancing and maintaining a tree's vigor and health.

Diagnostic DNA probes

The first step in addressing SOD is to ensure that the trees or plants are indeed infected by the SOD Phytophthora. The traditional approach is based on culturing the pathogen from the border of active infection. After a week or so, the pathogen can be identified in the laboratory based on its morphological traits. Unfortunately, culturing is not always successful, for instance when cankers become old or contamination occurs. This problem is common to Phytophthora species worldwide. Cases in which the pathogen is present but unculturable are called “false negatives.”

We have now developed DNA probes that will allow us to diagnose the pathogen's presence using Polymerase Chain Reaction (PCR) techniques, applied directly to host plant material. This molecular technique recently confirmed the identity of a fungal culture from rhododendron and its presence in several leaves of the same plant. PCR allows for samples to be processed in just a few hours and does not require a culturable stage of the pathogen, nor that the technician be trained in microscopic fungal morphology. The probe will not cross-react with any other Phytophthora species and will allow us to monitor our woodlands and plant nurseries in a more reliable and efficient way.

Inoculum control

Developing targeted inoculum control approaches such as sanitation and quarantine requires a refined understanding of the disease. In the case of a new disease such as SOD, lack of knowledge results in recommendations that may change as more information on the disease biology and epidemiology becomes available. Our current thoughts on SOD management recommendations are based on our present limited knowledge and on extrapolation from similar diseases, but have yet to be verified by specifically designed research studies.

The SOD Phytophthora grows optimally at 68°F (20°C) and is killed at temperatures higher than 95°F (35°C). This sensitivity to high temperatures may be a limiting factor in the inoculum production and therefore in the spread of the disease. All other species in the genus Phytophthora are favored by wet or moist periods, and it is likely that the same may be true for the SOD Phytophthora. For instance, we have observed that fungal sporangia present in the oozing sap in the late spring and early summer become undetectable during the dry summer months. In culture, the SOD Phytophthora produces abundant chlamydospores. In the case of related pathogens, these thick-walled propagules allow the disease agent to survive in soil, water and possibly wood. Although we still do not know where and for how long the SOD Phytophthora chlamydospores may survive, the most conservative approach would be to limit movement of all media that have been shown to harbor chlamydospores of similar pathogens.

The movement of media that potentially vector the disease (such as soil, wood, water and all horticultural material from infested areas) should be limited, particularly during wet periods when inoculum potential is at its highest and the climate may be most favorable to infection. Similarly, tree pruning and any other activity that may facilitate infection should be planned in hot, dry periods, when inoculum potential is at its lowest.

Given the high levels of local mortality, disposal of dead wood is extremely important. Because moist environments favor all Phytophthora species, treatments leading to rapid wood drying are likely to be beneficial. These treatments should decrease the amount of active inoculum present in the wood and may limit the risk of spreading the disease when transporting the wood. Studies are underway to determine the most appropriate way to treat wood; at present we recommend keeping it on the property where it was cut, to limit inoculum dispersal.

There are inherent costs attached to these guidelines aside from the added direct costs of managing for the disease. These costs range from loss of benefits derived from oak woodlands by the general public or land owners (such as limitation of firewood transport and use or limitation of recreational activities) to interference with the financial well-being of those who depend on oaks for their living (such as commercial plant nurseries located in areas of infestation, arborists and so on). Because of these costs, it is very important to verify through research exactly where and for how long the pathogenic inoculum survives. Although our concern is currently to avoid the spread of the disease to new areas, final long-term recommendations need to be based on the results of such research.

Chemical control

Chemical control approaches are routinely used in agriculture, but they have rarely been successfully adopted in trees, with the significant exception of orchard trees. Nevertheless, two successful fungicide treatments of oak diseases — one of which is caused by a Phytophthora species — (Fernandez-Escobar et al. 1999; Osterbauer et al 1994) are compelling evidence that such approaches may be integral components of a control strategy. Other Phytophthora species have been routinely controlled with the use of both fungicides and compounds such as phosphonates applied as foliar sprays or soil drenches, or injected into the trunks of trees. Almond, oak, avocado and cocoa trees have all shown remission or control of Phytophthora cankers in the medium or long term (Guest et al. 1995). It appears that such chemical treatments may be effective both for preventive and curative approaches (Browne and Viveros 2000).

Several compounds have already been tested and proven effective against SOD Phytophthora in the laboratory. Compounds that performed well in the in vitro tests are currently being used in field experiments. Compounds that may not perform well in vitro, but that are known to be effective in stimulating antifungal responses in planta are also being tested in the field. We believe that early treatment may be a key factor in chemical control of the disease.

Although the benefits of chemical treatments are often uncertain for trees, their costs may be many and far-reaching. The most significant costs include the side effects of any active compound used in the applications. Is the compound targeting only the specific pest or pathogen, or is it affecting many different categories of organisms, including humans? Which organisms does it affect the most? How does it disperse in the environment? How long will it be active against the target species and against other species? Will it accumulate in some organisms? Will the pathogen build up resistance easily or not? If resistance occurs, could it spread to other related pathogens?

These questions highlight the risks associated with chemical control, and prompt us to launch into chemical control strategies with the greatest caution. It is also possible that by prolonging the life of seriously compromised trees without a real remission of the disease, we may increase the frequency of other opportunistic tree pathogens that may affect not only the three oak species susceptible to SOD, but also other tree species. By keeping the tree alive for a longer period, we may also allow a longer availability of Phytophthora inoculum present in the bleeding cankers, which are likely to dry out faster upon tree death.

Future for molecular analysis

We are currently using genetic markers called Amplified Fragment Length Polymorphisms that will scan the whole genome of the organism. These will enable us to determine levels and patterns of genetic variability in populations of the pathogen. This information is essential in addressing important issues regarding the origin and the biology of the organism. The molecular information can be used to determine:

Potential for integrated approach

We believe that a complete approach, including practices to enhance tree health, early disease detection and targeted chemical treatment, may hold some promise for the control of SOD. Rotation of compounds is important to avoid the rise of resistance among populations of the primary pathogen. Chemical control of secondary SOD organisms may also be important. For instance, insecticide applications may be appropriate to protect trees that are on the threshold of becoming attractive to beetles, to prolong their lives while other approaches are undertaken against the primary SOD pathogen.

Although fungicides may eventually prove useful in managing this disease, the mode of compound delivery and the potential for resistance buildup are serious concerns. The potato industry in the Northwest, for instance, has been seriously impacted by the rise of resistance to the widely used compound metalaxyl. The onset of resistance in P. infestans, the causal agent of late potato blight, was the result of sexual mating between pathogenic isolates from different world regions.

Such a complex integrated approach appears feasible for landscape and garden trees, but unfortunately not for trees in woodland situations. Ultimately, the fate of the oak species affected by SOD will be determined by the levels of disease resistance present in natural populations of these trees. We hope that a significant portion of oak populations will display signs of resistance both to infection by the SOD pathogen and to SOD mortality. For the time being, we recommend that SOD-infected trees not be prematurely cut down. The three oak species affected by SOD depend on resistant individuals to build up their populations, which are being decimated by this new disease.