DOI: 10 .1564/15apl12 Outlooks on Pest Management – Apri l 2004 85

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An emergent plant disease is uniting the European and theNorth American continents, its name, Sudden Oak Death(SOD) may be puzzling to most Europeans, as indeed,mortality of native oaks has not been widely reported inEurope. Historically, this disease owes its name to the rapidcrown decline of SOD-affected trees observed in Californiain the early 1990s. Ironically, the most susceptible Californiatrees are not oaks, but tanoaks a related species belonging tothe genus Lithocarpus. California red oaks and intermediateoaks were subsequently identified as highly susceptible toSOD, displaying similar symptoms, e.g. bleeding trunks andrapid browning of the entire crown. In 2000, two significantevents marked the history of SOD research: the discovery ofthe causal agent behind SOD and the unexpected findingthat the same agent had been previously isolated not frombleeding trees, but from blighted ornamental rhododendronsin Germany. The microbe in question was at that time stillundescribed, but it was subsequently named Phytophthoraramorum.

The genus Phytophthora is certainly a familiar one forpathologists and tree care specialists as it includes well-known plant pathogens, causing diseases in trees defined bydescriptive names such as ink disease or gummosis.

Why then, is there so much concern in both continents,about this emergent disease? The answer lies in the levels ofdestruction this microbe has caused locally in California. Insome sites, 100% of the mature tanoaks and 45% ofCalifornia coast live oaks have been killed by P. ramorum,with obvious ecological and socio-economical consequences.To compound the seriousness of the SOD issue, P. ramorumis inevitably little understood since it has been recentlydiscovered. Unfortunately, it appears to be an oddball in theworld of forest Phytophthoras. While most forest Phytoph-thoras in the temperate world are root-infecting soil-borneand water-borne-organisms, P. ramorum spreads mostlyaerially and generally infects trees and plants above the soilline, while maintaining the soil-borne and water-bornefeatures of its close relatives. In light of the actualdevastation caused by SOD in California, and because of thehigh levels of uncertainty, due to our limited knowledge ofthe biology of the causal agent, there is great concernsurrounding the presence of P. ramorum in nurseries. Infes-tations in nurseries have been reported in most EuropeanUnion countries, in Washington State, in British Columbia(Canada) and in Oregon State, where natural infections in alimited portion of a single county are actively being curtailedby a proactive eradication program. The discovery in 2003

of individual trees killed by SOD in Europe in correlationwith the previous planting of infected rhododendrons hasreaffirmed the need for active management of this disease.

…“Same but different”…While irrefutable evidence pointing to a putative exoticnature of P. ramorum in both continents is still lacking, mostscientists agree SOD seems to have the features of anemergent, i.e. ‘new’, disease. The high levels of mortalityrecorded in California are reminiscent of high mortalitylevels caused by exotic diseases such as chestnut blight,Dutch elm disease, and white pine blister rust. The causalorganism and the disease have never been described before,and a more in depth genetic analysis of North American andEuropean populations, revealed that there is limited geneticvariability in each continent, another typical trait of intro-duced diseases. P. ramorum requires individuals bearing twodifferent mating types (A1 and A2) in order to complete itssexual cycle. In nature in North America, only A2individuals have been reported until now, while – with asingle exception – only A1 have been reported from nurseryor nursery-linked infections in Europe. DNA analysis hasshown that the European and the North Americanpopulations are genetically very distinct and represent twolineages that are not intermixing with each other. Thisgenetic distinction is also matched by different traits such asgrowth rate, morphology and differential pathogenicity on arange of hosts. Presumably, both mating types and represen-tatives of both lineages would be present in the area whereP. ramorum originated: the location of this area still eludesthe world scientific community.

In nurseries of the Pacific Northwest, individualsbelonging to both mating types and lineages were discoveredin 2003; in plants adjacent to one another. The A1 and A2isolates were shown to be interfertile in the laboratory,These findings are troubling for two reasons: a) TheEuropean lineage is, as stated above, genetically quitedifferent from the North American one and could cause asecond different wave of SOD; and b) The two lineagescould mate and generate progeny with new traits, thanks tosexual recombination events.

The presence of sexual activity may turn P. ramorum intoa formidable adversary; even without sex, this organism hasbeen able to colonize entire forests. P. ramorum in factproduces large amounts of asexual infectious propagules.Genetic analyses have shown that a single clone has

SUDDEN OAK DEATH: A TALE OF TWO CONTINENTS

Matteo Garbelotto, Extension Specialist and Adjunct Professor, Department of Environmental Science, Policy and Management, University of California, Berkeley, CA, USA describes this new disease of oaks andrelated trees and compares the infection potential in the US and Europe

SUDDEN OAK DEATH

colonized most of California, while a larger variety of clonesis present in European nurseries. At times, nurseries indifferent countries share the same clone: clearly indicating P.ramorum is traded with its hosts among nurseries. Thefinding that some North American nurseries are infested byboth lineages is strongly suggestive of the role played by theindustry in unknowingly aiding the movement and maybeeven the introduction of this pathogen in the continent.

The biology of P. ramorum and the symptomsof SODInfestations in nurseries and in the wild (with the exceptionof the vast spread of California coast already colonized bythe pathogen) have been treated very aggressively with aslash/burn/spray approach. Despite these strong efforts, trueeradication of the pathogen has not always been possibleboth in the wild and in nurseries. One of the reasons for thelimited success of these operations may be due to the limitedunderstanding of the life cycle of the pathogen. Here is asummary of our knowledge of the pathogen’s biology, basedmostly on studies of diseased forest areas in California. Thelife cycle of the pathogen in forests elsewhere, or in artificialenvironments such as commercial nurseries, may differ

significantly from what is described in this section. Weatherpatterns and host composition will necessarily have a hugeimpact on the epidemiology of the disease.

Early symptomsIn order to fully understand SOD, we need to removeourselves from the implicit preconception that the disease is

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Figure 1. Sudden oak death lesion on a bay laurel leaf (Laurusnobilis) (Photo courtesy of Matteo Garbelotto)

Figure 3. Characteristic bleeding on a coast live oak (Photocourtesy of Matteo Garbelotto)

Figure 2. An exposed canker under the bleeding bark on a tanoak in the Big Sur (Photo courtesy of Matteo Garbelotto)

“sudden”, that it affects mostly “oaks” and that it is always,or almost, “deadly”. It is estimated that a few years (two ata minimum) may be required for the disease to causemortality at any infested site. In nature, infestations aredriven by plant hosts that can be infected easily and supportsporulation of infectious and/or resting propagules.Epidemiologically important hosts in California include inorder of importance, bay laurel leaves (Umbellulariacalifornica, Lauraceae), tanoak twigs and leaves(Lithocarpus densiflora, Fagaceae) and redwood needles(Sequoia sempervirens, Taxodiaceae). The importance ofthese hosts is exemplified by the fact that, with a singleexception, all infested California sites, are characterized bythe presence of bay laurel and/or tanoaks. Circumstantialevidence points to rhododendrons and camellias as potentialimportant artificial hosts for the disease, possibly linking theornamental industry and the wild land components of SOD.Leaves and twigs of these and other susceptible hosts arereadily colonized by swimming zoospores carried in amicroscopic oval-shaped structure called sporangium. Thesporangium can be airborne and once it lands on a suitablehost surface it will release the zoospores. The presence of afilm of water on the plant surface for several hours seems togreatly facilitate the infection process. Warm temperatures

(around 18–20°C) also seem to be ideal for infection. Onceinfected, leaves and twigs develop black lesions oftenmarked by a darker line, called a reaction zone. Reactionzones are more marked in hosts that, at least temporarily,can block off the growth of the pathogen. Species that areextremely susceptible (e.g. some Rhododendron species) donot normally display reaction zones, but the margin of thelesion is rather diffuse. In conditions of high humidity (closeto 100%) and moderate temperature, new sporangia andresting round structures called chlamydospores will beproduced on the lesions in approximately 48 hours.Chlamydospores produced by other Phytophthora specieshave been shown to be resting structures that allow for thesurvival of the pathogen during harsh weather conditions,but their role for P. ramorum is still unclear. These eventsmark the end of the initial stage of disease and the beginningof the second phase.

Second phase of the diseaseInfestations will most likely be driven by the epidemiologi-cally important hosts, but once in a site, the pathogen iscapable of infecting a very broad range of hosts includingtrees and shrubs, woody and herbaceous perennials. In

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Figure 4. A tan oak killed by sudden oak death (Photo courtesyof Matteo Garbelotto)

Figure 5. Dead coast live oaks at China Camp in Marin County(Photo courtesy of Matteo Garbelotto)

addition, re-infection of individual plants is a most likelyoccurrence. In some hosts leaf infection is accompanied bybranch infections causing typical branch die-backsymptoms: in the second phase of the disease leaf lesionsmay proceed into the stems and vice versa leading toobvious die-back symptoms such as those observed forinstance in tanoaks, rhododendrons, Pacific madrones(Arbutus menziesii, Ericaceae), Toyons (Heteromelesarbutifolia, Rosaceae), Pacific huckleberry (Vacciniumovatum, Ercaceae). In some hosts, including bay laurel,maple spp. (Acer), buckeye (Aesculus californica, Hippocas-tanaceae) only leaves are affected. Infectious propagules willalso accumulate in the soil and water streams: soil and waterare bound to play an important epidemiological role,especially when factoring in human fruition andmanagement of woodlands. It has already been shown thatleaves of susceptible hosts will become infected whensplashed with infected soil. On the other hand, whathappens at the interface between roots and infested soilawaits further research. Although dead and fallen leavesappear to loose infectiousness quite rapidly, they alsocontribute to increase the inoculum potential of the soil andwater.

The third and the final phases of SODIn the next disease phase, the main stems of tanoaks andoaks may be infected. Although infection appears to occurin the absence of any visible wound, P. ramorum maychoose the path of least resistance, whether lenticels or otheropenings in the bark. The pathogen colonizes preferentiallythe sugar-rich phloem of the host, while only marginallycolonizing the outer bark and the xylem. As a result ofphloem colonization, a canker develops under the bark, andsappy exudates will flow outside the bark. Aerial seeps notconnected to the root collar are good indications that a treehas been infected by P. ramorum. Other Phytophthoraspecies, in fact, can cause identical seeps, normally thoughlinked to root or root collar infection. It is noteworthy tomention that multiple cankers, at different heights, are oftenvisible on tanoaks. These cankers are thought to be startedby sporangia produced on leaves and twigs of the same oradjoining plants. On the more resilient coast live oak trees,cankers are normally found in the lower part of the bole,presumably where sporangia accumulate, or in areasadjacent to sources of sporangia, e.g. infected bay leaves.Coast live oak leaves and twigs, in fact, are never or rarelycolonized by P. ramorum. Although the production of toxinsby P. ramorum has not been excluded yet, it is believed thatthe main effect of the disease on oaks and tanoaks is girdlingof the cambium. Upon girdling, the irreversible deathprocess is started, but it may take a year or more, before thebrowning of the crown becomes apparent.

Significant girdling of the tree circumference marks thebeginning of the last phase of the disease, characterized bythe presence of secondary organisms and opportunisticpathogens. Bark and ambrosia beetles are attracted by thesedying trees, and a variety of wood decay fungi and cankerrots can develop freely on the moribund specimens. At thelandscape level, this phase is characterized by the removal of

the most susceptible species including not only oaks andtanoaks, but also other plant hosts.

Epidemiological notesAreas with wet climates and constant mild temperatures,resembling the central California coast are optimal todisease development. Most of the sporangia production inCalifornia occurs during the rainy season (December toJune). In the dry season, sporangia production is reduceddramatically, and as the soil dries, P. ramorum in the soilbecomes non-viable, whether permanently or temporarily isstill unclear. The pathogen can be recovered all year roundin streams, indicating that sporulation is also occurring allyear round and the pathogen is viable when it is in favorableenvironments.

The disease spreads almost exclusively where epidemio-logically important, or foliar hosts, are available. The levelsof mortality appear to be correlated with incidence of foliarhosts: maximum levels of mortality in tanoaks are observedwhere both tanoaks and bay laurels are present, while coastlive oak mortality is positively correlated with abundance ofbay laurel trees. There is no record of SOD from areaswhere coast live oak grows without bay laurel. It has beenrecently shown that some populations of bay laurels are lesssusceptible to infection by P. ramorum than others. In theabsence of other foliar hosts, areas characterized by thesemore resistant bay trees should be less prone to epidemic-levels of SOD. Additionally, in each one of seven coast liveoak populations tested, some individual oaks consistentlyappeared to be “slow-cankering” when challenged with thepathogen in artificial inoculation studies on cuttings. Thistrait has been also observed in nature, where a few treeshave survived for several years despite being infected.

Sporangia will be effectively airborne for 5 metres; thus,increased spacing among trees may slow down the spread ofthe disease. P. ramorum will sporulate on the epidemiolog-ical important hosts listed above, but also on many of itsfoliar hosts: two native California roses were just found tobe infected and able of supporting sporulation. Sporulationdoes not seem to be important on the bark of oaks andtanoaks, but it is triggered in debarked wood. Theabundance of foliar hosts in California and the ability to bespread aerially for short distances can easily explain localinfestation, but rarer long distance events, or movementaided by animals and humans have to be invoked to explainthe overall range of the pathogen, which stretches for over300 miles along the California coast. Predictions of SOD inEurope are hinged on the understanding of which hosts maybe significant sources of infection, and which hosts may bedeadly affected by the disease. As in California, white oakshave been shown to be relatively resistant to P. ramorum,while Mediterranean live oaks and European beech werehighly sensitive to the pathogen when tested in thelaboratory. North American red oaks are also widelyplanted in the old continent; most species belonging to thisgroup of oaks are highly susceptible to the disease. In thecase of Europe, interregional transport of the diseaseappears to have already occurred through the trading andsales of ornamental plants.

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A case of “do or die”? Emerging managementoptions for SODPreventing the introduction of P. ramorum into new areasshould be the first priority when managing SOD. Thisentails identifying the most likely sources of infection: inorder of importance these sources may be live plants, greenwaste, soil and water, debarked untreated wood, entire logsor firewood. Plants supporting sporulation are obviouslymore likely to start new infestations than ones that do notdo so. For non-live substrates, moisture content is indeed adecisive factor in determining potential risk associated withthe substrate. The drier the substrate, the less likely it is tobe contagious; it should be noted, however, that if thesubstrate supports sporulation, it may become highlyinfectious upon being re-hydrated. Wood chip from coastlive oak for instance can be easily sanitized by air-drying atroom temperature, while bay leaves – which supportabundant sporulation – require heat treatment in order to besanitized.

Green waste is normally composed of both woody andleaf debris and should be considered infectious if originatingfrom an infested area. Prolonged exposure (> than 7 days) totemperature of 55°C, or composting have been shown tosanitize these substrates effectively; the jury is still outregarding mulching as a sanitation tool. Some specificprotocols used by the spice industry combine in a 22 hourtreatment progressive heating to 55°C and a moderatevacuum, again effectively killing the pathogen in bay leaves.As mentioned above, soil can be infectious, and theelimination of soil particles from vehicles, shoe soles, paws,or arborist tools is essential and potentially more importantthan the actual surface sterilization of tools or tires usingbleach or lysoform solutions. The use of infested water maybe an issue in forests where water is drawn from creeks fordust abatement. When P. ramorum gets into the water inrecycling systems of nurseries, it can be recovered with easefrom the water, providing a convenient source of infection.

Once infection is established, an obvious strategy is thatof decreasing the amount of infection at a site. This may beachieved by elimination of infected plants or plant parts, bypartial removal of top soil and litter, especially under plantsknown to be infected, and in the case of nurseries, by the useof contact fungicides like copper derivatives or metalaxyl.Fungicides though are bound to simply mask the presence ofthe pathogen. In our experience, even metalaxyl caused onlya maximum of 50% reduction in viability. The second stepconsists in slowing down the epidemic: this can be achievedin a variety of ways: spacing between foliar hosts should beincreased, combination of foliar and terminal hosts (e.g.

oaks and bay laurel) should be avoided, recycled watershould be treated, movement of soil avoided, drip irrigationshould be preferred to overhead irrigation, early morningirrigation and decreased shading levels should beimplemented to avoid long hours of water accumulation onplant surfaces. Fertilization should be avoided, as P.ramorum favors succulent fast grown tissue. Managementoperations such as plant removal should be carried outduring cold spells or dry periods, when the pathogen is leastactive. Wounds in tree areas exposed to inoculum may becolonized promptly by P. ramorum: small branch pruning ofoaks for instance rarely increases infection levels, as they arenot likely areas for sporangia accumulation, but largerwounds and pruning of major branches, may increaseinfection by P. ramorum.

Oaks and tanoaks at risk can also be treated usingphosphites. Two registered treatments are available inCalifornia, and work optimally in a preventive way:injection in the outer xylem and topical application ofphosphites combined with an organosilicate surfactant-penetrant. In both cases, the compound is systemicallytranslocated and broken down into phosphonic acid, theactive ingredient that triggers a defense response by theplant. Research has shown that these treatments willeffectively prevent infection and slow down the growth of P.ramorum cankers. Other treatments aimed at coating thebark of trees with a contact fungicide were not shown to beeffective. Phosphite treatments will not kill the pathogen,but only slow it down, and are designed to be administeredon a yearly basis. Foliar treatments of oaks and tanoaksusing phosphites only provided a short-lived enhancedresistance, and caused significant phytotoxicity. In Australiathough, many plant species respond well to foliartreatments: this may be a further option available toEuropeans.

For further readings I recommend to log on www.suddenoakdeath.org and check all the information and linksavailable there.

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Matteo Garbelotto is an Extension Specialist and Adjunct Professor ofForest Pathology and Mycology in the Department of EnvironmentalScience, Policy and Management of the Ecosystem Sciences Divisionat the University of California at Berkeley, where he has studiedsudden oak death following its outbreak in California.