sudden oak death syndrome fells 3 oak...

CALIFORNIA AGRICULTURE, JANUARY-FEBRUARY 2001 9

New pests and plant diseases

Sudden oak death syndromefells 3 oak speciesMatteo Garbelotto ❏ Pavel Svihra ❏ David M. Rizzo

Sudden oak death syndrome killed about 350 coast live oak trees in this area near MillValley in Marin County. This photo was taken in March 2000.

Sudden oak death” refers to acomplex set of symptoms that hasalready culminated in the death oftens of thousands of Californiaoak trees. Now confirmed inseven coastal counties, SOD at-tacks California tanoak, coast liveoak and California black oak. Al-though several fungal species andthe western oak bark beetle andambrosia beetles have been asso-ciated with the syndrome, we nowhave solid evidence that a newlydiscovered Phytophthora speciesis the primary causal agent.

This Phytophthora species wasrecently isolated in rhododendronas well; it may be the same spe-cies that was isolated, but not de-scribed, on rhododendrons inGermany in 1993. The discoveryof SOD on rhododendron has seri-ous implications. The disease maywell be present at the ecosystemscale, and its appearance on an or-namental plant suggests the possi-bility of wider dissemination.

A team of UC scientists has de-veloped an integrated approach tomanaging this disease, includingpractices to enhance tree health.Early disease detection and tar-geted chemical treatment mayalso hold some promise for dis-ease management. In addition, wehave developed a molecular probethat will enable rapid identificationof SOD from any infected part ofthe plant. Ultimately, the fate ofthe oak species affected by SODwill be determined by the levels ofdisease resistance present innatural populations of these trees.

“

10 CALIFORNIA AGRICULTURE, VOLUME 55, NUMBER 1

A coast live oak tree displaying bleedingcankers. These cankers are normally thebest diagnostic feature of trees affectedby sudden oak death syndrome and arecaused by a newly discovered species ofPhytophthora.

This is a micrograph of theyet-to-be-namedPhytophthora species.

Exudate from a canker mats in moss on acoast live oak.

Ray

Mor

itz

Since 1995, mortality of at least three native Califor-nia oak species has reachedepidemic levels (McPhersonet al. 2000). The seeminglyrapid decline of these trees istriggered by a new species ofPhytophthora (a funguslike or-ganism). Named sudden oakdeath (SOD), or oak mortalitysyndrome, this disease hasnever before been observedin California. SOD has re-

ceived substantial attention by the me-dia and the public because oaks notonly represent a major component ofmany California forest ecosystems,they are also important both in urbanlandscapes and at the urban/rural in-terface. Tanoak, coast live oak andblack oak trees are distributed along1,500 miles of the California and Or-egon coast. Researchers, land manag-ers and policy-makers are using adap-tive management to direct theirefforts, but are faced with the chal-lenge of formulating control guide-lines based on a limited and stillevolving understanding of the disease.

This article summarizes the currentknowledge about sudden oak deathand refers to some of the ongoing ex-periments designed to provide in-sights into its possible causes. Finally,we address potential options for con-trol. Because this work is in progress,most of this information should betreated as preliminary. Often we relyon references to similar but not identi-cal problems in other systems. The in-formation presented here has beencondensed from the work of many re-

searchers actively in-volved in the study ofSOD. Among them areSusan Frankel, Tho-mas Gordon, KentJulin, Maggi Kelly,Steve Koike, BriceMcPherson, NicolePalkowsky, GareySlaughter, AndrewStorer, Ted Swiecki,Steve Tjosvold, EllieRilla, Rick Standifordand David Wood.

What is sudden oak death?

Sudden oak death (Svihra 1999) isknown to affect three tree species:California tanoak (Lithocarpusdensiflora), coast live oak (Quercusagrifolia) and California black oak (Q.kelloggii). We have also isolated thepathogen from rhododendrons. Al-though SOD has been reported only incentral and northern coastal California(fig. 1), the natural range of tanoaksand black oaks extends well into theinterior ranges of California and intoOregon. Coast live oak is foundthroughout Southern California andinto Baja California, Mexico. In addi-tion, the presence of SOD on a com-mercial ornamental plant (rhododen-dron) raises the possiblity that it mayalready have been disseminated morewidely than we know. Its presence inornamental plants could be tempo-rarily masked by the use of fungicides.

We still do not understand patternsand mechanisms of dispersal of thisnew disease. Therefore it is not knownwhether SOD will expand throughoutthe range of its hosts, or whether itsdistribution will be limited by factorssuch as climate, presence of competingorganisms and predators, or absenceof potential vectors. The disease is cur-rently patchy in its regional distribu-tion, but can affect 40% to 80% of treesin any given stand. Such high levels ofoak mortality are unprecedented inCalifornia, and suggest the emergenceof a new disease.

Trees affected by SOD display arange of symptoms depending onstage of infection, tree species and thetime of year. Wilting of apical shoots isa common initial symptom of infectedtanoaks. Sparse pale-green foliage is


DelNorte

SiskiyouModoc

Humboldt

Trinity Shasta

Marin

SanMateo

Santa Cruz

Lassen

Tehama

MendocinoSierra

Plumas

Sut

ter

ButteGlenn

Colusa

Lake

Nevada

PlacerYuba

YoloNapaSonoma

El Dorado

Sacra-mento

SolanoSanJoaquinContra

CostaAlameda

SantaClara

Amador

Calaveras

Tuolumne

Alpine

Mono

Stanislaus

Merced

Madera

Mariposa

SanBenito

Monterey

FresnoInyo

TulareKings

San LuisObispo Kern

San Bernardino

Santa Barbara

VenturaLos Angeles

Orange Riverside

San Diego Imperial

SanFrancisco

Confirmed cases of SOD

Fig. 1.Countiesinfected with thenew species ofPhytophthora thatcauses sudden oak deathsyndrome (SOD).

S.O.D. Phytophthora basics

observed in coast live oaks in an ad-vanced stage of the syndrome. Maturetrees of all three host species affectedby SOD display bleeding and sunkencankers on the bole, or trunk. Thesecankers are more frequent on thelower part of the trunk, but they canbe found up to 30 feet (10 meters) fromthe base of the tree. Cankers seep adark brown or amber-colored sap.Such seeping is the most dependablesymptom of a tree affected by SOD. In-tensity of seeping varies among differ-ent trees and may fluctuate on the

same tree, perhaps depend-ing on the time of year orstage of canker development.For instance, seeping tends todecrease during dry periodsand in older cankers. Insmaller tanoaks, no seepingmay be associated with thecankers, which appear water-soaked and may be scatteredon stems.

In later stages of SOD, coal-blackdome-shaped fruiting bodies of thefungus Hypoxylon thuorsianum invari-ably develop. At first the black fungaldomes appear near and above the can-ker areas and then over large portionsof the bole. Beetles (Coleoptera:Scolytidae) are also consistently foundon trees in later stages of SOD. Thewestern oak bark beetle(Pseudopityophthorus pubipennis) andambrosia beetle (Monarthrum spp.)feed respectively on the bark (phloem)and sapwood of host trees. Their feed-ing activity results in barely visibletunnels on the tree bark and in theproduction of finely ground frass(chewed phloem or sapwood) that ac-cumulates, often in large amounts, onthe tree bark. We believe that in spiteof the strong association betweenHypoxylon and/or beetles and treemortality, these organisms should beconsidered as secondary. Such organ-isms are present on declining oaksworldwide, no matter what the cause ofthe decline.

We have isolated an oomycete fun-gus belonging to the genus Phyto-phthora from many trees with SODsymptoms. Many oomycetes are ag-gressive plant pathogens, includingthe pathogen responsible for the infa-mous Irish potato blight of the 19thcentury. We succeeded in isolatingPhytophthora from SOD-related seep-ing cankers at the root crown to over10 feet (3 meters) above the ground.Seeping, a likely host defense re-sponse, may provide the fungus with apotential route of dispersal for its in-fectious propagules. These pro-pagules, called sporangia, have beenfound in the sap oozing from cankersduring wet and cool periods. Fromthere, the sporangia may either besplashed onto other trees or possiblytransported by animals. Infection on a

new host begins in the phloem,progresses to the cambium and even-tually reaches the xylem. The phloemis often a bright red with numerousthin black lines that delimit the canker.Infection and discoloration are alwaysmore extensive in phloem tissues thanin xylem. Black discoloration can ex-tend up to 3/4 inch (2 cm) into the xy-lem below the bleeding canker. Discol-oration in the phloem and xylem mayextend up to 20 inches (50 cm) in alldirections from the point of bleeding.Phytophthora is typically isolated fromthe margins of these discolored areas,although it can often be isolated fromolder portions of the cankers. Cankerson smaller tanoaks are not as distinct,and zone lines are not always appar-ent in either phloem or xylem.

Elevated oak mortality caused byother species in the genus Phytophthorahas been reported from other regionsof the world (Brasier et al. 1993, Junget al. 1999, Tainter et al. 2000). For de-cades, a few Phytophthora species (P.cinnamomi, P. citricola and P. cactorum)have been known to be present onoaks in California. However, thenewly isolated Phytophthora does notmatch the morphology of any of theknown described species (Erwin andRibeiro 1996), and is still unnamed. Inthis paper, we refer to this new species

Phytophthora species produce both sexuallyand asexually, and the gametes and clonesthat result can survive as spores for extendedperiods, even in adverse environments.

In the new SOD Phytophthora, onlyasexual structures have been observed todate. This may be favorable. Pathogens with-out the ability to recombine their genetic infor-mation through mating can be aggressive butare less capable of rapidly adapting to new en-vironments or hosts.

Scientists have observed that this speciesproduces two types of infectious structurescalled sporangia and chlamydospores, bothcapable of being detached from the main bodyof the pathogen. It follows that spread may oc-cur through air, water, soil or animals. How-ever, actual methods of transmission have notbeen confirmed in the field.

The following definitions are derived fromAinsworth’s Dictionary of the Fungi, with addi-tions by the authors relevant to SOD.

Chlamydospore: A thick-walled asexualspore made by the rounding up of one or morecells. It can survive for up to several monthsor years in unfavorable conditions. It is knownto be responsible for long- and medium-rangemovement in contaminated soil and water ofmany pathogens including the Port Orford ce-dar Phytophthora.

Oosphere: The female gamete, similar tothe “egg.”

Oospore: The resting spore from a fertil-ized oosphere. The structure is the result ofmating and genetic recombination.

Sporangium: An organ producing asexualspores. It is not the result of mating; no geneticrecombination occurs. In this case it is lemon-shaped and the spores have two flagella(whiplike extensions for movement). The spo-rangium can detach itself from the body of thepathogen, germinate directly and infect thehost without the need to open up and releasethe zoospores.

Zoospores: Asexual spores with flagella.(In virtually all Phytophthora species, flagellaenable spores to swim; they can move towardssusceptible infection sites by following chemi-cal signals from the plant.) If they do not find asusceptible host they can encyst for variableperiods of time and wait for more favorableconditions. They do not survive for more thana few days, however.

continued on p. 13


Identifying the character and causeof sudden oak death (a previouslyundescribed Phytophthora species)was a tortuous, 5-year process.

It began in April 1995 whenhomeowners asked the UC Coopera-tive Extension office in MarinCounty to investigate the dieback ofmore than a dozen tanoaks border-ing a creek. The root crown area be-neath the bark of the largest tanoakshowed mats and strands of “shoe-strings” that are typical of the oakroot fungus, Armillaria mellea. Theseoaks are usually tolerant of thispathogen and can withstand somedrought. However, it was thoughtthat prolonged drought from 1990 to1992, followed by very wet years in1993 and 1994, might have reducedthe vigor of tanoaks, allowing A.mellea to infect and kill them.

In June 1996, a reexamination ofthe dying tanoaks revealed a shock-ing number of dying and dead trees,not only along a creek but also on theslope and along the crest of a hill.Symptoms could no longer be attrib-uted to A. mellea. The current year fo-liage of other trees had turned yel-low-green and new shoots drooped,typical of trees with root disease.Trees exhibited bleeding cankers andheavy infestations of ambrosiabeetles, signalled by piles of finewhite-to-tan sawdust on the lowertrunks. Dead trees also had charcoal-black spherical fungal fruiting bodieson the bark surface.

With the cooperation of arborists,horticulturists and pathologists, in-tensive sampling of affected treeswas conducted in June, August andOctober 1996. Samples of discoloredtissues and wilted twigs were sent toUC and state laboratories, but nocause was identified. Scientists pro-posed that the mysterious diebackcould be caused by the devastatingchestnut blight Cryphonectriaparasitica, or perhaps oak wilt causedby Ceratocystis fagacearum. Again,

Diagnosis of SOD: case study of a scientific processPavel Svihra

laboratory tests followed, but neitherfungus was detected.

Coast live oak dieback

In May 1997, the first coast liveoaks, Quercus agrifolia, began to die ingardens of Marin County. The deadtrees were also experiencing stressfulenvironmental conditions. The coastlive oak symptoms were strikinglysimilar to those of dying tanoaks, es-pecially the heavy ambrosia beetle in-festations, and the growth of a char-coal-colored hemispheric fungus onthe bark. However, scientists alsonoted that some young tanoaks died inthe vicinity of mature, dead tanoakswithout noticeable bleeding or ambro-sia beetle attacks.

In June 1997, we examined two MillValley tanoaks that were 6 inches indiameter, adjacent to each other, andthe targets of initial ambrosia beetle at-tacks. The first tree died during thewinter season; the second had yellowfoliage with typical wilted shoots.Both trees were uprooted with a back-hoe. Samples were collected of ne-crotic or discolored roots, inner bark,and cambium tissues under thepatches of ooze, and branches andshoots that showed discoloration,streaks or staining. Three fungi andone bacterium were identified in labo-ratory tests, but none of these organ-isms was considered by plant patholo-gists to be the primary agent of treemortality.

About the same time, the CaliforniaDepartment of Food and Agriculturelaboratory identified three beetlesfrom infested trunk sections: two am-brosia beetles and one bark beetle.

Characterization and control

During the fall and winter of 1997many more dead trees appeared. Asno pathogen could be causally impli-cated in the dieback, which continuedto expand, UC Cooperative Extensionin Marin County formulated manage-ment recommendations in spring 1998.

It seemed probable that drought fol-lowed by excessive rains had causedstress in the affected trees. As a result,bark beetle and ambrosia beetle popu-lations built up in dying tanoaks to anepidemic stage. The new beetle gen-erations not only attacked tanoaks butalso shifted their attacks to coast liveoaks. Through meetings and work-shops with arborists, UCCE’s MarinCounty office implemented a programof prophylactic insecticidal sprayscombined with tree health care (irriga-tion, cleaning of root crown areas,pruning, fertilization, etc.).

In June 1998, soon after the treat-ment program began, there was a sub-stantial increase in dead coast liveoaks from Mill Valley to Novato, andtwo black oaks, Quercus kellogii, diedin Novato. The symptoms of the blackoaks were almost identical to those ofdying tanoaks and coast live oaks. Forthe first time, the word “epidemic”was used widely and the CE advisorinformed the media. However, scien-tists did not agree on the definition ordiagnosis for the problem becausenew inconsistencies continued toemerge. For example, bark beetles andambrosia beetles were considered theprimary cause of the death in coastlive oaks and black oaks because thesetrees were predisposed by environ-mental stress. However, the death ofvery young tanoaks that lacked oozeon the trunk and were not attacked bybeetles seemed to contradict insects asthe primary cause. It appeared that anunknown pathogen was traveling frommature dead trees to kill these youngtrees.

Rising tree deaths

In winter 1999 the number of dyingtrees continued to rise into the tens ofthousands. A San Rafael residentcounted 316 dead trees on MountainView Avenue. At the same time, anopinion circulated that the oak die-back was a temporary phenomenon (a“natural cycle”) related to climatic ex-


The coal-black dome-shaped fruiting bodies of the fungus Hypoxylon thuorsianum.

Jack

Kel

ly C

lark

tremes. In June 1999, the California For-est Pest Council met to assess the mas-sive death of oaks. Cooperating plantpathologists uprooted a symptomatictanoak tree and collected samples. Noplant pathogens were recovered. Several“Pest Alerts” were published (Svihra1999, 1999a, 1999b, 2000). One describedthe syndrome as “sudden oak death,”and the term stuck.

Scientific breakthrough

In June 2000, David Rizzo, UC As-sistant Professor of Plant Pathology,sampled infected coast live oaks in theChina Camp State Park near SanRafael and returned to his laboratoryon the same day to make isolationsfrom the tissue samples. A fungus ofthe Phytophthora genus was isolatedfrom the tissue and appeared to be theunderlying cause of SOD (McPhersonet al. 2000). This rapid processing of tis-sue samples was essential to recovery ofthe pathogen. Previous samples thatwere mailed or even hand-deliveredhad not revealed the cause.

Currently, there are no measuresavailable that will alter the underlyingdisease. The potential for fungicides,other management practices and wooddisposal to mitigate the impact of thedisease is currently under investiga-tion. In vitro studies have demon-strated that some fungicides may slowdown or prevent the underlying dis-ease development process. However,the effectiveness of these and other con-trol methods have not yet been con-firmed in the field, nor have potentialproblems of resistance been assessed.

ReferencesSvihra P. 1999. Sudden Death of Tanoak,

Lithocarpus densiflorus. UC Cooperative Ex-tension. Pest Alert #1, June. 2 p.

Svihra P. 1999a. Western Oak BarkBeetles and Ambrosia Beetles, Killers of LiveOaks. UC Cooperative Extension. Pest Alert#3, June. 2 p.

Svihra P. 1999b. Western Oak BarkBeetles and Ambrosia Beetles, Killers of LiveOaks. UC Cooperative Extension. Pest Alert#3A:1-4. October.

Svihra, P. 2000. Protection of Live OaksAgainst Attacks by Oak Bark Beetles andAmbrosia Beetles. UC Cooperative Exten-sion. Pest Alert 3B:1-4, January.

McPherson BA, Wood DL, Storer AJ, et al.2000. Oak Mortality Syndrome: SuddenDeath of Oaks and Tanoaks. Tree Notes 26(August). 6 p.

as SOD Phytophthora. DNA analysisalso indicates that this is a newundescribed species, whose only closerelative is another Phytophthora species(P. lateralis), which is present only inCalifornia, Oregon and Washington.This related pathogen, considered bymany to be an exotic species, is ex-tremely virulent on Port Orford cedar(Chamaecyparis lawsoniana) in the Pa-cific Northwest. Although the two spe-cies of oomycetes are morphologicallydifferent and attack different tree spe-cies, they share the same requirementfor cool climates; they do not toleratetemperatures over 95°F (35°C). Bothspecies also produce similar chlamyd-ospores, thick-walled propagules thatensure survival of the pathogen inharsher climatic conditions or unfa-vorable environments.

The role played by chlamydosporesand most of the biology of the SODPhytophthora is still unknown.Phytophthora lateralis and many otherPhytophthora species are dispersedthrough the movement of soil and wa-ter contaminated by chlamydospores.This mode of dispersal needs to beverified for the SOD species. Whetherand for how long the pathogen cansurvive in dead wood is also still un-determined. Although our observa-tions indicate that the pathogen can in-fect trees by penetrating directly

through the unbroken bark, the impor-tance of wounds and of potential vec-tors needs to be investigated.

One feature that appears to differ-entiate the SOD Phytophthora fromother forest Phytophthora species is thepresence of an aerial component. Thiscomponent, inferred from the presenceof aerial cankers, can be determined bythe cauducous nature of the sporangia.This feature may allow these infectiouspropagules to detach from the fungalcolony and become airborne. A signifi-cant aerial component in the diseasecycle may also explain the lack of a strictassociation between patterns of diseasespread and the presence of water. Suchassociation is normally observed fornonaerial Phytophthoras.

Understanding whether the SODpathogen may be (a) introduced; (b) anew taxonomic entity obtained by hy-bridization between P. lateralis and an-other Phytophthora species; or (c) a na-tive pathogen may help in predictingthe final impact that SOD is going tohave on oak ecosystems. Non-nativeor new diseases often find plant hostsill-equipped to defend themselves,and the result can be host decimation.Native diseases may cause epidemicsdue to increased host predisposition, butthey rarely wipe out entire host species.

We also do not know whether ornot this pathogen completes its sexual

continued from p. 11


1009080706050403020100

1009080706050403020100

Per

cen

tag

e o

f tr

ees

cm

Mortality Seepingcankers

Beetleattacks

DBH ofdead trees

DBH of all trees

AstroNon-Astro

a a

a a

a

b

a a aa

Fig. 2. Comparisons between 67 treestreated with the insecticide Astro and 67untreated trees in a coast live oak stand.At the end of a 4-month period, new oakmortality and the number of trees withseeping cankers were not significantly dif-ferent between the two treatments. Datafrom the two treatments were comparedwith either chi square or t-test analyses.Different letters indicate statistical signifi-cance at P = 0.05. DBH = diameter atbreast height.

cycle. In general, pathogens that arecapable of completing the sexual cycleare more successful both in adaptingto new environments and in develop-ing resistance to compounds used forchemical treatments.

Probable primary causal agent

Although SOD may ultimately bethe result of a complex scenario inwhich several pathogens, pests andabiotic factors interact with one an-other, the new Phytophthora seems tobe found on all trees affected by SOD.This was evidenced by direct isola-tions of the pathogen from the hosts orby the presence of typical sunken can-kers and seeping. This strong associa-tion suggests that this organism is theprimary causal agent of the syndrome.Inoculations of seedlings, saplings andadult trees have been performed toconfirm its pathogenicity. Preliminaryresults from all three experiments in-dicate that this oomycete is capable ofcausing disease symptoms on inocu-lated hosts comparable to those innaturally infected plants.

Although there is also a strikingcorrelation between SOD and bothHypoxylon and beetle attacks, we be-lieve that these and other organismsmay play a secondary role. Fungi inthe genus Hypoxylon are normallyendophytically present and inactive inthe host, until mechanical damage, in-sects or diseases create the right envi-ronmental conditions for their growth.Twig or stem cankers caused by fungiother than Phytophthora (for example,

Botryosphaeria spp.) are also oftenabundant in areas affected by SOD.These are considered as secondary oropportunistic organisms that thrive ontrees weakened by other factors. Thecorrelation between insect attacks anddead trees is striking, and much re-mains to be understood about the roleplayed by insects. Although it is un-disputed that insects speed the deathrate of trees, it is unclear whether theyare significant vectors for the patho-gen and necessary to kill trees.

Although vectoring by beetles orother insects cannot be excluded atthis point, our observations indicatethat many cankers are initiated with-out any sign of beetle activity. Thereare also many cases in which smalltrees, although unsuitable for coloni-zation by such insects, are infected bythe new Phytophthora species and die,again suggesting a secondary roleplayed by insects in SOD.

Marin County field study

In March 2000, 67 coast live oakswere sprayed with the insecticideAstro (36.8% active ingredientpermethrin), according to label direc-tions, on the lower 12 feet (4 meters) oftree boles on a Marin County ranchheavily affected by SOD. Only live trees(both healthy and symptomatic) weretreated and marked. Trees with ex-tremely thin crowns and abundant signsof beetle activity were regarded as deadand therefore excluded from treatments.

In July 2000, we returned to the siteand performed a comparative evalua-tion of the 67 treated trees (Astrogroup) versus 67 untreated trees (non-Astro group) in an adjacent stand.None of the trees in the Astro group dis-played signs of beetle activity on thetreated portions of the boles, while 11(16%) of the non-Astro trees showedsymptoms of beetle attacks (fig. 2).

The two groups were well suited fora comparison:

(a) Both groups occupy a similararea (approximately 2 acres) and in-clude trees of comparable size (fig. 2);

(b) The groups were adjacent andhad identical topography;

(c) The groups were similar foresttype, with the majority of trees eithercoast live oak or California bay;

(d) Both groups were subject to

comparable inoculum levels and expe-rienced a significant level of SOD-caused mortality during the trial pe-riod (fig. 2).

The overall mortality at the studysite (that is, including all 134 treesfrom the Astro and the non-Astrogroups) was approximately 13% (17individual trees). The number of seep-ing cankers showed that the levels ofinfection were not different betweenAstro-treated and nontreated groups(fig. 2). A total of 9 trees (13%) in theAstro group were dead, despite thenotable absence of bark beetles andambrosia beetles in the treated portionof the trunk. All of the dead trees inthe Astro group were mature, and hadbeen killed without the presence ofbark beetles. However, all dead treesdisplayed Phytophthora-caused bleed-ing cankers, providing strong supportof Phytophthora as the primary causalagent of SOD. Furthermore, levels ofmortality were not significantly differ-ent between the two groups (fig. 2),providing further evidence that insectswere not the primary cause of SOD-linked mortality. Finally, all trees inthe non-Astro group attacked bybeetles (11) also had bleeding cankers,but 22 other trees displayed bleedingcankers without signs of beetle activ-ity. This result reinforces the observa-tion that cankers precede beetle at-tacks, and that fungal colonization is afactor predisposing trees to attacks bybark and ambrosia beetles.

Both inoculation tests and this beetle-exclusion study point to Phytophthora asthe most likely primary agent of SOD inCalifornia. Nevertheless, secondaryagents including insects and otherpathogens are bound to play a signifi-cant role. For instance, it has been re-ported that insecticide applications de-lay tree mortality for several months(Svihra 2000). This information clearlyindicates that insect attacks stronglycontribute to accelerated tree death.Our current challenge is to understandthe basic biology of the SOD Phytoph-thora in relation to the plant hosts and tothe other agents involved in SOD. An ef-fective control strategy will be feasibleonly when the sequence of possible in-teractions among all damaging agents isbetter understood.

continued on p. 16


The OakMapper Web site allows users toreport locations of SOD-infected trees.

As of January 2001, sudden oak death(SOD) had been confirmed by labora-tory isolations in six coastal counties,and reported in several others. Earlyestimates of tree loss indicate that 40%to 80% of the oaks or tanoaks in someareas are affected and likely to die.

Establishing the baseline conditionsof SOD and monitoring its spread overthe next 5 to 10 years will be critical.The California Oak Mortality TaskForce (COMTF) was established in Au-gust 2000. One of its goals is to deter-mine appropriate methods for moni-toring the SOD epidemic. The taskforce’s monitoring committee is pursu-ing multi-scale strategies and ap-proaches, utilizing numerous datasources. Researchers with UCBerkeley’s Center for the Assessmentand Monitoring of Forest and Environ-mental Resources (CAMFER) are tak-ing the lead in the monitoring effort.

Regional-scale monitoring. Weare using regional-scale monitoring todetermine the overall extent and rangeof SOD; roadside and aerial surveysare helping to determine its geo-graphical extent. Trained field staffvisited the sites of reported extensiveoak mortality to take samples of af-fected trees, prior to lab confirmation,in order to determine the most likelycurrent zones of infestation. To date,sampling from areas outside thesezones has not revealed additional ar-eas of SOD.

We are also gathering informationabout individual symptomatic treesusing the OakMapper Web site. Thissite, developed by CAMFER, usesWebGIS (geographic informationsystems) technology to allow interac-tive map browsing and submissionof the location and condition of trees.This is a valuable tool in developingthe regional picture of SOD. Areaswhere SOD is confirmed can be moreintensely sampled, guided by new

Multi-scale approaches takento SOD monitoring

Nina Maggi Kelly ❏ Brice A. McPherson

submissions of oakmortality.

Landscape-scalemonitoring. The condi-tions and spatial pat-terns of dead and dyingtrees are crucial indica-tors of disease progres-sion. Patterns of spatialvariation of thesyndrome’s progres-sion through a standcan serve as a key diag-nostic tool, illuminatingpossible mechanisms of transmissionamong trees and interactions amongcausal agents. For example, clumpeddistributions could indicate that thedisease is spread through roots or el-evated insect populations, rather thansoil-related or climatic effects. Spreadthat follows topography would indi-cate the predominance of root infec-tions via movement of moisturethrough soil. An increasingly sparsespatial pattern, or a pattern coincidingwith hiking trails or hoofed wildlifecorridors, might indicate the impor-tance of human or wildlife vectors.

Remotely sensed data (primarily re-flected light in the visible and near in-frared portions of the spectrum, inte-grated over a discrete area) is avaluable tool for determining the con-dition and pattern of trees with SOD.Airborne Data Acquisition and Regis-tration (ADAR) imagery was acquiredfor two study areas in Marin Countyby Positive Systems, Inc. Digital imag-ery was acquired at 1 meter groundspatial resolution in blue, green, redand NIR light. While the imagery isstill being processed, preliminary re-sults indicate that in the hardwoodforests of China Camp State Park inMarin County, this data can discrimi-nate between dead and dying treesand determine spatial patterns. The re-sulting maps can be linked to fire

spread models. This type of workshould be employed in other locations,particularly where SOD is in the early-infection stage. Because tanoak islargely an understory species, theremay be some problems identifying thecondition and pattern of dead trees insome areas.

Local-scale monitoring. We estab-lished research plots in Marin Countyto follow symptomatic and healthytrees. Plots were established in Marchand April 2000, in China Camp StatePark (CCSP), near San Rafael, and inMarin Municipal Water District(MMWD), a protected watershed adja-cent to Mt. Tamalpais. These plotswere selected to encompass a diversityof habitat types and tree species. Coastlive oaks and California black oaksgrow in both sites, but tanoaks areonly found in MMWD. Ten plots wereestablished in each of these sites, for atotal of 20 plots and approximately 750trees.

All oaks and tanoaks greater than 2inches dbh (diameter at breast height)are included in the survey. Each tree isevaluated for seeping, bark beetles,Hypoxylon fungus and foliage appear-ance. Plots are evaluated at 2- to 3-month intervals.


SOD Web sitesCalifornia Oak Mortality Task Force

http://suddenoakdeath.orgIntegrated Hardwood Range

Management Program (IHRMP)http://danr.ucop.edu/ihrmp/

UC SOD research team updateshttp://camfer.cnr.berkeley.edu/oaks

OakMapperhttp://camfer.cnr.berkeley.edu/oaks/map-intro.htm(Interactive Web-based GIS distribution maps.)

Confirmed SOD siteshttp://camfer.cnr.berkeley.edu/oaks/#distribution.

Distribution graphicshttp://camfer.cnr.berkeley.edu/oaks/#maps(Downloadable maps includingcurrent SOD distribution andoaks at risk.)

Remote-sensing resultshttp://camfer.cnr.berkeley.edu/oaks/ADARinfo.html(ADAR image analysis of twostudy areas in Marin County.)

Marin County UC Extensionhttp://cemarin.ucdavis.edu

Integrated management approach

We have just begun to unravelsome of the dynamics of SOD, and re-search and outreach professionals arehard pressed to provide control strate-gies that may lead to disease contain-ment or remission. The three main is-sues of disease management pertain toour ability to (a) prevent furtherspread of the disease; (b) contain dis-ease intensity where it is alreadypresent; and (c) identify treatments ca-pable of arresting or remitting diseasedevelopment on infected trees.

Even though cures have rarely beendeveloped for tree diseases, it is notunrealistic to envision a combinationof cultural and chemical treatmentsthat may prove effective against thespread of SOD. The extent of controldepends largely on the type of strate-gies available and on their costs, botheconomic and environmental. Themore targeted and less costly the ap-proach, the broader its application. Itis also important to keep in mind thatlandscape trees may display symp-toms identical to SOD, but be infectedby Phytophthora species other than theSOD Phytophthora. A precise diagnosisis therefore essential, because otherPhytophthora-caused diseases requiredifferent control approaches. Further-more, all SOD control strategies mustbe accompanied by general practicesaimed at enhancing and maintaining atree’s vigor and health.

Diagnostic DNA probes

The first step in addressing SOD isto ensure that the trees or plants areindeed infected by the SODPhytophthora. The traditional approachis based on culturing the pathogenfrom the border of active infection. Af-ter a week or so, the pathogen can beidentified in the laboratory based onits morphological traits. Unfortu-nately, culturing is not always success-ful, for instance when cankers becomeold or contamination occurs. Thisproblem is common to Phytophthoraspecies worldwide. Cases in which thepathogen is present but unculturableare called “false negatives.”

We have now developed DNAprobes that will allow us to diagnosethe pathogen’s presence using Poly-

Considerable between-plot varia-tion was found in infection rate andmortality at both CCSP and MMWD.Through December 2000, the between-plot range of coast live oaks exhibitingseeping was 8% to 95% (CCSP) (35%

average) and 3% to 56% (MMWD)(21% average). For tanoaks in MMWD,the between-plot range was 18% to80% (55% average). Estimates of mor-tality in the plots are limited to treesthat show clear evidence of seepingcankers prior to death. For coast liveoak in CCSP, estimated mortalityacross all plots ranged from zero to21% (12% average). In MMWD, coastlive oak mortality across all plots waszero to 32% (7% average). The corre-sponding values for tanoak were zeroto 26% (14% average). No infected val-ley oak were identified.

We are continuing monitoring at allscales, including evaluating satelliteremote-sensing at the regional scale,more high-resolution mapping at thelandscape scale, and statistically validfield surveys at the local scale. We arehopeful that these efforts will make avaluable contribution to ongoing re-search in order to find a solution forSOD.

N.M. Kelly is Cooperative ExtensionSpecialist and B.A. McPherson isPostdoctoral Researcher, Department ofEnvironmental Sciences, Policy andManagement, UC Berkeley. Kelly is co-director of CAMFER and chair of theCOMTF monitoring committee;McPherson is a member of the COMTFmonitoring committee.

Classified ADAR imagery, draped over topography. Red areas are dead treecrowns. Image produced by Kalliopi Tzivanaki of UC Berkeley Department of Envi-ronmental Sciences and Policy Management.

continued from p. 14


Red frass left by western oak bark beetleboring into phloem and xylem of coast liveoak. Western oak bark beetle can be foundon trees in later stages of sudden oakdeath syndrome.

Adult western oak bark beetle.

Jack

Kel

ly C

lark

Jack

Kel

ly C

lark

merase Chain Reaction (PCR) tech-niques, applied directly to host plantmaterial. This molecular technique re-cently confirmed the identity of a fun-gal culture from rhododendron and itspresence in several leaves of the sameplant. PCR allows for samples to beprocessed in just a few hours and doesnot require a culturable stage of thepathogen, nor that the technician betrained in microscopic fungal mor-phology. The probe will not cross-react with any other Phytophthora spe-cies and will allow us to monitor ourwoodlands and plant nurseries in amore reliable and efficient way.

Inoculum control

Developing targeted inoculum con-trol approaches such as sanitation andquarantine requires a refined under-standing of the disease. In the case of anew disease such as SOD, lack ofknowledge results in recommenda-tions that may change as more infor-mation on the disease biology and epi-demiology becomes available. Ourcurrent thoughts on SOD managementrecommendations are based on ourpresent limited knowledge and on ex-trapolation from similar diseases, buthave yet to be verified by specificallydesigned research studies.

The SOD Phytophthora grows opti-mally at 68°F (20°C) and is killed attemperatures higher than 95°F (35°C).This sensitivity to high temperaturesmay be a limiting factor in the inocu-lum production and therefore in thespread of the disease. All other speciesin the genus Phytophthora are favoredby wet or moist periods, and it islikely that the same may be true forthe SOD Phytophthora. For instance, wehave observed that fungal sporangiapresent in the oozing sap in the latespring and early summer become un-detectable during the dry summermonths. In culture, the SODPhytophthora produces abundantchlamydospores. In the case of relatedpathogens, these thick-walledpropagules allow the disease agent tosurvive in soil, water and possiblywood. Although we still do not knowwhere and for how long the SODPhytophthora chlamydospores may sur-vive, the most conservative approachwould be to limit movement of all me-

dia that havebeen shown toharbor chlamy-dospores of simi-lar pathogens.

The move-ment of mediathat potentiallyvector the dis-ease (such assoil, wood, waterand all horticul-tural materialfrom infested ar-eas) should belimited, particu-larly during wetperiods when inoculum potential is atits highest and the climate may bemost favorable to infection. Similarly,tree pruning and any other activitythat may facilitate infection should beplanned in hot, dry periods, when in-oculum potential is at its lowest.

Given the high levels of local mor-tality, disposal of dead wood is ex-tremely important. Because moist en-vironments favor all Phytophthoraspecies, treatments leading to rapidwood drying are likely to be benefi-cial. These treatments should decreasethe amount of active inoculum presentin the wood and may limit the risk ofspreading the disease when transport-ing the wood. Studies are underway todetermine the most appropriate wayto treat wood; at present we recommendkeeping it on the property where it wascut, to limit inoculum dispersal.

There are inherent costs attached tothese guidelines aside from the addeddirect costs of managing for the dis-ease. These costs range from loss ofbenefits derived from oak woodlandsby the general public or land owners(such as limitation of firewood trans-port and use or limitation of recre-ational activities) to interference withthe financial well-being of those whodepend on oaks for their living (suchas commercial plant nurseries locatedin areas of infestation, arborists and soon). Because of these costs, it is veryimportant to verify through researchexactly where and for how long thepathogenic inoculum survives. Al-though our concern is currently toavoid the spread of the disease to newareas, final long-term recommenda-

tions need to be based on the results ofsuch research.

Chemical control

Chemical control approaches areroutinely used in agriculture, but theyhave rarely been successfully adoptedin trees, with the significant exceptionof orchard trees. Nevertheless, twosuccessful fungicide treatments of oakdiseases — one of which is caused by aPhytophthora species — (Fernandez-Escobar et al. 1999; Osterbauer et al.1994) are compelling evidence thatsuch approaches may be integral com-ponents of a control strategy. OtherPhytophthora species have been rou-tinely controlled with the use of bothfungicides and compounds such asphosphonates applied as foliar spraysor soil drenches, or injected into thetrunks of trees. Almond, oak, avocadoand cocoa trees have all shown remis-sion or control of Phytophthora cankers


Left, pale sawdustlike am-brosia beetle frass andseeping bark typical ofSOD on coast live oak.Above, an adult ambrosiabeetle and frass from tun-neling into heartwood.Right, an adult ambrosiabeetle.

Jack

Kel

ly C

lark

Jack

Kel

ly C

lark

Jack

Kel

ly C

lark

Future for molecular analysis

We are currently using geneticmarkers called Amplified FragmentLength Polymorphisms that will scanthe whole genome of the organism.These will enable us to determine lev-els and patterns of genetic variabilityin populations of the pathogen. Thisinformation is essential in addressingimportant issues regarding the originand the biology of the organism. Themolecular information can be used todetermine:■ If it is more likely that the patho-

gen is introduced (little variabil-ity) or native ( a lot of variability).

■ Whether the pathogen goesthrough a sexual stage. If so, andif there is significant genetic vari-ability in the population, thepathogen may evolve through re-combination. This may be pivotalin formulating control strategies.

■ More knowledge about theorganism’s epidemiology andlong range movement. If thepathogen population is the same

in the medium or long term (Guest etal. 1995). It appears that such chemicaltreatments may be effective both forpreventive and curative approaches(Browne and Viveros 2000).

Several compounds have alreadybeen tested and proven effectiveagainst SOD Phytophthora in the labo-ratory. Compounds that performedwell in the in vitro tests are currentlybeing used in field experiments. Com-pounds that may not perform well invitro, but that are known to be effec-tive in stimulating antifungal re-sponses in planta are also being testedin the field. We believe that early treat-ment may be a key factor in chemicalcontrol of the disease.

Although the benefits of chemicaltreatments are often uncertain fortrees, their costs may be many and far-reaching. The most significant costs in-clude the side effects of any activecompound used in the applications. Isthe compound targeting only the spe-cific pest or pathogen, or is it affectingmany different categories of organ-

isms, including humans? Which or-ganisms does it affect the most? Howdoes it disperse in the environment?How long will it be active against thetarget species and against other spe-cies? Will it accumulate in some or-ganisms? Will the pathogen build upresistance easily or not? If resistanceoccurs, could it spread to other relatedpathogens?

These questions highlight the risksassociated with chemical control, andprompt us to launch into chemicalcontrol strategies with the greatestcaution. It is also possible that by pro-longing the life of seriously compro-mised trees without a real remission ofthe disease, we may increase the fre-quency of other opportunistic treepathogens that may affect not only thethree oak species susceptible to SOD,but also other tree species. By keepingthe tree alive for a longer period, wemay also allow a longer availability ofPhytophthora inoculum present in thebleeding cankers, which are likely todry out faster upon tree death.


across its range in California, wehave to infer medium range move-ment either by itself or vectoredby animals and/or humans. If iso-lates in Europe and California areconfirmed to be the same, modesof intercontinental spread wouldhave to be inferred.

Potential for integrated approach

We believe that a complete ap-proach, including practices to enhancetree health, early disease detection andtargeted chemical treatment, may holdsome promise for the control of SOD.Rotation of compounds is important toavoid the rise of resistance amongpopulations of the primary pathogen.Chemical control of secondary SODorganisms may also be important. Forinstance, insecticide applications maybe appropriate to protect trees that areon the threshold of becoming attrac-tive to beetles, to prolong their liveswhile other approaches are under-taken against the primary SODpathogen.

Although fungicides may eventu-ally prove useful in managing this dis-ease, the mode of compound deliveryand the potential for resistancebuildup are serious concerns. The po-tato industry in the Northwest, for in-stance, has been seriously impacted bythe rise of resistance to the widelyused compound metalaxyl. The onsetof resistance in P. infestans, the causalagent of late potato blight, was theresult of sexual mating betweenpathogenic isolates from differentworld regions.

Such a complex integrated ap-proach appears feasible for landscapeand garden trees, but unfortunatelynot for trees in woodland situations.Ultimately, the fate of the oak speciesaffected by SOD will be determined bythe levels of disease resistance presentin natural populations of these trees.We hope that a significant portion ofoak populations will display signs ofresistance both to infection by the SODpathogen and to SOD mortality. Forthe time being, we recommend thatSOD-infected trees not be prematurelycut down. The three oak species af-fected by SOD depend on resistant in-

dividuals to build up their popula-tions, which are being decimated bythis new disease.

M. Garbelotto is Forest Pathologist, De-partment of Environmental Sciences,Policy and Management, Ecosystem Sci-ences Division, UC Berkeley; P. Svihra isHorticulture Advisor, UC CooperativeExtension, Marin County; and D.M.Rizzo is Plant Pathologist, Department ofPlant Pathology, UC Davis.

The authors are also indebted to themany volunteers and students who mademuch of this research possible. The fieldexperiment, the in vitro fungicide tests,and some of the inoculation trials wouldnot have been possible without the help ofMr. Ralph Zingaro. They are also gratefulto Susan Frankel and the U.S. Forest Ser-vice for funding provided through a coop-erative agreement between UC and the Pa-cific Southwestern region of the ForestService.

ReferencesBrasier CM, Robredo F, Ferraz JFP. 1993.

Evidence for Phytophthora cinnamomi in-volvement in Iberian oak decline. Plant Pa-thology (Oxford). 42(1):140-5.

Browne GT, Viveros M. 2000. Chemicalmanagement of lethal Phytophthora cankerson almond. Phytopathology 90:S10.

Erwin DC, Ribeiro OK. 1996.Phytophthora Diseases Worldwide. St. Paul,MN: American Phytopathological Society.

Fernandez-Escobar FJBR, Gallego M,Benlloch M et al. 1999. Treatment of oak de-cline using pressurized injection capsules ofantifungal materials. European J Forest Pa-thology 29(1):29-38.

Guest DI, Pegg KG, Whiley AW, et al.1995. Control of Phytophthora diseases oftree crops using trunk-injected phosphonates.Hort Reviews 17:299-330.

Jung T, Cooke DEL, Blaschke H, et al.1999. Phytophthora quercina sp. nov., caus-ing root rot of European oaks. MycologicalResearch 103:785-98.

McPherson B, Wood DL, Storer AJ, et al.2000. Oak Mortality Syndrome: SuddenDeath of Oaks and Tanoak. Calif Dept For-estry and Fire Protection, Tree Note # 26.

Osterbauer NK, Salisbury T, French DW,et al. 1994. Propiconazole as a treatment foroak wilt in Quercus alba and Q. macrocarpa.J Arboriculture 20(3):202.

Svihra P. 1999. Sudden death of Tanoak,Lithocarpus densflora. Pest Alert #1, UC Co-operative Extension. 2 p.

Svihra P. 2000. Protecting Live OaksAgainst Bark Beetles and Ambrosia Beetles.Pest Alert #3B, UC Cooperative Extension,Marin County. 4 p.

Tainter FH, O’Brien JG, Hernandez A, etal. 2000. Phytophthora cinnamomi as a causeof oak mortality in the state of Colima,Mexico. Plant Disease 84:394-8.

Oak trees that are planted in lawns often get overwatered, which leads to their decline.This type of oak mortality is sometimes mistaken for sudden oak death syndrome.

sudden oak death syndrome fells 3 oak...

Documents