A

v

Sudden Oak Death and 

Phytophthora ramorum: 

A Summary of the 

Literature 

2010 Edition

John T. Kliejunas 

United States 

Department of 

Agriculture

Forest Service

Pacific Southwest 

Research Station

General Technical Report

PSW-GTR-234

September 2010

DEPAR TMENT OF AGRICULT URE
Author

John T. Kliejunas, retired; former regional forest pathologist, U.S. Department of 

Agriculture, Forest Service, Pacific Southwest Region, Vallejo, CA.

Opinions expressed may not necessarily reflect the position of the U.S. Department 

of Agriculture.

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not imply endorsement by the U.S. Department of Agriculture of any product or 

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registered. All uses of pesticides must be registered by appropriate state or federal 

agencies, or both, before they can be recommended.

CAUTION: Pesticides can be injurious to humans, domestic animals, desirable 

plants, and fish or other wildlife if they are not applied properly. Use all pesticides 

selectively and carefully. Follow recommended practices for the disposal of surplus 

pesticides and pesticide containers.

Cover photo: Photo by Stephen Joseph Photography, Pleasant Hill, California.

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endorsement by the U.S. Department of Agriculture.

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Abstract

Kliejunas, John T. 2010. Sudden oak death and Phytophthora ramorum: a summary of the literature. 2010 edition. Gen. Tech. Rep. PSW-GTR-234. Albany, 

CA:. U.S. Department of Agriculture, Forest Service, Pacific Southwest Research 

Station. 181 pages.

Sudden oak death and Phytophthora ramorum, both first recognized about a decade 

ago, have been the subject of hundreds of scientific and popular press articles. This 

document presents a comprehensive, concise summary of sudden oak death and 

P. ramorum research findings and management activities. Topics covered include 

introduction and background, identification and distribution, the disease cycle, 

epidemiology and modeling, management and control, and economic and environmental impacts.

Keywords: Sudden oak death, Phytophthora ramorum, invasive species, tanoak, 

coast live oak, mixed-evergreen forests. 
Contents

1 Chapter 1. Introduction and Background

9 Chapter 2. Causal Agent, Distribution, Hosts, Diagnosis

31 Chapter 3. The Disease Cycle

55 Chapter 4. Modeling Disease Distribution and Spatial-Temporal 

 Patterns of Mortality

71 Chapter 5. Management and Control

107 Chapter 6. Economic and Environmental Impacts of 

 Phytophthora ramorum

122 Acknowledgments

122 English Equivalents

123 References
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Chapter 1: Introduction and Background

First Reports

An unusual die-off of tanoaks (Lithocarpus densiflorus (Hook. & Arn.) Rehd.) 

in the Mill Valley/Mount Tamalpais area of Marin County, California, was first 

documented in April 1995 (Svihra 1999b, 1999c, 2001), when homeowners reported 

scattered patches of dying tanoaks—with entire crowns dead and with bleeding 

basal cankers—to Pavel Svihra, University of California (UC) Cooperative Extension. The symptoms were also being reported by arborists and others on nearby 

tanoaks, including those at Muir Woods National Monument, and farther south 

in coastal Santa Cruz County and around Big Sur (Monterey County) in the same 

year. Heavy ambrosia beetle attacks and black fruiting bodies of a Hypoxylon

fungus, later identified as Hypoxylon [Annulohypoxylon] thouarsianum (Swiecki 

2001), were associated with the dying trees. 

Undetermined Cause

Attempts by arborists, pathologists, and horticulturists to determine the cause of the 

die-off yielded only several saprophytic micro-organisms (including Armillaria sp., 

Hypoxylon [Annulohypoxylon] sp., Pseudomonas tolaasii and Diplodia quercina) 

(Svihra 1999a), and identification of two ambrosia beetles (Monarthrum scutellare and M. dentiger) and one bark beetle (the western oak bark beetle, Pseudopityophthorus pubipennis) from affected tanoaks. The micro-organisms identified 

and the beetles are considered secondary or opportunistic, attacking only stressed 

trees. It was postulated by some that several years of drought from 1990 to 1992 

followed by excessively wet years (El Niño) in 1993 and 1994 resulted in tree stress, 

allowing the secondary fungi and beetles to attack the weakened trees, with bark 

beetle and ambrosia beetle populations subsequently building up to unprecedented 

levels (Hagen 1999; Svihra 1999a, 2001). Other stress factors—including overstocking, fire exclusion, construction, incompatible landscaping, and others—were also 

suggested as contributing to the die-off (Hagen 1999).

Epidemic Spread

By May 1997, not only tanoaks, but also coast live oaks (Quercus agrifolia Née) 

were dying in the Marin Municipal Water District lands and in China Camp State 

Park on San Francisco Bay (Svihra 2001). The symptoms on coast live oaks (seeping or bleeding areas on the trunk followed by fading of the foliage, beetle attack, 

and appearance of Hypoxylon fruiting bodies) were similar in appearance to those 

of dying tanoaks. 
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GENERAL TECHNICAL REPORT PSW-GTR-234

By spring 1998, beetle attacks on coast live oaks were resulting in a rapid 

increase of dying coast live oaks (Svihra 1999b, 1999c), and several California 

black oaks (Q. kelloggii Newb.) in the Novato area (Marin County) were reported 

with similar symptoms. Although the dominant thinking was that the primary 

cause of the widening mortality was bark and ambrosia beetles attacking stressed 

trees, some scientists noted that young tanoaks without oozing trunk cankers or 

beetle attacks were also dying, suggesting that an unknown pathogen was involved 

as the primary stress agent rather than drought followed by high rainfall.

Public Concern

The rapid spread of the disease in 1998, in an urban-wildland interface area 

inhabited by millions of people, heightened public concern. The highly visible 

disease was killing trees on public and private lands, threatening residential and 

forest land, parks, industries, water supply, soil retention, and wildlife. Weakened 

and dead trees were a hazard because they could fall, destroying life and property. 

They also posed a severe fire hazard. The unabated mortality, now being described 

as epidemic, increased through 1999 (McPherson and others 2000). Concerned 

homeowners pressed county supervisors, administrators, and politicians for investigation and treatment.

Because the causal agent was unknown at the time, the syndrome was commonly referred to after the most obvious symptoms—the trees dying in a somewhat 

sudden fashion. A University of California (UC) Cooperative Extension publication 

(Svihra 1999b) described the crown symptoms as appearing rather suddenly, resulting in rapid death. The mortality was referred to as “sudden oak death” in a second 

UC Cooperative Extension publication (Svihra 1999a) and the term was picked up 

by others, notably the press, to describe the phenomenon. 

In 1999 a multidisciplinary research team of UC scientists was formed to 

address the cause and management options for control of sudden oak death. A 

23-person team was formed, including forest pathologists, forest entomologists, 

ecologists, silviculturists, wildlife biologists, remote sensing/geographic information system experts, and urban forestry/arboriculture experts from UC Davis and 

UC Berkeley, and advisors from UC Cooperative Extension county offices. Funds 

were provided by both UC and the U.S. Department of Agriculture, Forest Service 

(USDA FS). The UC system provided $70,000 in emergency funding, and the 

USDA FS, Forest Health Protection provided $85,000 for research and monitoring. 

Susan Frankel, plant pathologist, then with the Pacific Southwest Region of the 

USDA FS, was instrumental in focusing and coordinating early efforts. 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

In June 2000, the Marin County Board of Supervisors passed a resolution 

declaring that sudden oak death had created a state of emergency. “We are in the 

midst of a catastrophe,” Supervisor Cynthia Murray stated at the time (San Francisco Chronicle Nov. 5, 2000). Several months later, under the leadership of the 

California Forest Pest Council and the California Department of Forestry and Fire 

Protection, local, state, and federal agencies joined to form what would become, 

in August 2000, the statewide California Oak Mortality Task Force (COMTF). 

Involved early on were the California Department of Forestry and Fire Protection, 

the California Forest Pest Council, UC, and the USDA FS. The advisory group, 

chaired by Susan Frankel, undertook the challenge of establishing a cooperative, 

unified approach and offering guidance to funders, lawmakers, management agencies, research institutions, and others concerned with the disease. In November of 

that year, the state of California appropriated $100,000 for use by the newly formed 

COMTF, and federal officials announced that an additional $1 million would 

become available for research, monitoring, and outreach (San Francisco Chronicle 

Nov. 2, 2000). In Oregon, pathologists from the Oregon Departments of Agriculture 

and Forestry, Oregon State University (OSU), and the USDA FS formed a less 

formal coordinating group, and initiated sudden oak death (SOD) detection surveys 

in the southern part of the state.

From the beginning, political leaders and their constituents in the densely 

populated San Francisco Bay area of California were concerned. Efforts to obtain 

funding were fruitful largely because of the public outcry and media coverage 

that the new problem received and technical guidance of the COMTF. California’s 

2001–2002 state budget contained $3.6 million to address sudden oak death in 

the state, with the funds to be administered through the California Department of 

Forestry and Fire Protection, and the COMTF serving in an advisory capacity. At 

the federal level, $2.4 million ($1.4 million from a Federal Emergency Supplemental 

Appropriation, and $1 million from the USDA FS) was made available in 2002 for 

research, monitoring, and management projects.

Causal Agent Found

The availability of funding and similarity of the bleeding canker symptoms to those 

caused by species of Phytophthora elsewhere (Erwin and Ribeiro 1996) renewed 

efforts to find a causal agent (Garbelotto and Rizzo 2005). In June 2000, David 

Rizzo, UC Davis, consistently isolated a Phytophthora species from bleeding 

cankers on oaks and tanoaks at different locations. By early fall, Koch’s postulates 

(criteria used to establish causal agent) had been completed on seedlings through 
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GENERAL TECHNICAL REPORT PSW-GTR-234

artificial inoculations, and by late fall 2000, inoculation experiments on adult oaks 

and tanoaks were successfully completed (Garbelotto and others 2001, Rizzo and 

others 2002b). Inoculated trees developed large girdling stem cankers that started 

bleeding approximately a month after inoculation. Hypoxylon and beetles became 

visible on the trees only after the Phytophthora-caused lesions developed in the 

bark. Now that a cause was known, forces were focused on obtaining information 

on the causal organism.

In October 2000, British plant pathologist Clive Brasier, United Kingdom Forestry Commission, was visiting with Dr. Everett Hansen at OSU. At the conclusion 

of that visit, Dr. Brasier traveled to the San Francisco area to observe the impacted 

forests and the newly isolated Phytophthora. While there, he was shown laboratory 

cultures of the unidentified Phytophthora isolated from cankers. Several weeks 

after his return to the United Kingdom, Dr. Brasier heard a description of a new and 

unnamed Phytophthora species from rhododendron in Germany and the Netherlands isolated in 1993 (Werres and Marwitz 1997) and noted a striking similarity 

with the cultures he had been shown in California.

In Europe, the organism was at that time known only as a pathogen causing leaf 

blight and branch dieback of Rhododendron spp. and root collar cankers on Viburnum spp. This knowledge led California researchers to isolate a Phytophthora from 

rhododendron with leaf symptoms in a Santa Cruz container nursery surrounded by 

dying oak woodlands, in December 2000. The cultural morphology was identical to 

that of the sudden oak death Phytophthora, and by January 2001 Matteo Garbelotto, 

UC Berkeley, confirmed that the ITS (internal transcribed spacer) DNA sequence 

of isolates obtained from rhododendrons in that Santa Cruz County nursery was 

identical to that of isolates obtained from oaks (Garbelotto and Rizzo 2005). A 

later study (Mascheretti and others 2008), using microsatellite analysis techniques, 

determined that P. ramorum made its first appearance in California forests at two 

separate sites, one in Mount Tamalpais in Marin County and the second in Scotts 

Valley in Santa Cruz County. Forest strains of P. ramorum were identical to strains 

found in nurseries near the two sites about the same time, providing evidence that 

P. ramorum entered California via the nursery trade. 

When researchers from California and Europe exchanged pathogen ITS 

sequences, a perfect match of the sequences from isolates collected in Germany 

and the Netherlands and from isolates collected in California was found (Garbelotto 

and Rizzo 2005). In April 2001, the pathogen was formally named Phytophthora

ramorum Werres, de Cock, & In’t Veld sp. nov. (Werres and others 2001).
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Increased Spread and Public Concern 

In North America

The discovery and naming of the pathogen was an essential step, but the problem 

in the United States continued to increase in intensity and concern. New hosts for 

P. ramorum—including California bay laurel (Umbellularia californica (Hook. & 

Arn.) Nutt.) and coastal redwood (Sequoia sempervirens (D. Don) Endl.)—were 

being reported with increasing frequency (the 2009 host list includes 109 plant species), and the pathogen was discovered in July of 2001 in a forest location in Curry 

County, Oregon. Attempts to eradicate that pathogen there on 2,400 acres of forest 

have cost $4.3 million through 2008 (Kanaskie and others 2010a). The extensive 

range of hosts and the spread of the pathogen will be covered in chapter 2.

In early 2001, the state of Oregon issued an emergency rule banning host plants 

and other plant products coming from California unless they had been treated. A 

few months later, the Oregon quarantine became permanent (March 27, 2001), and 

Canada issued a similar quarantine (March 9, 2001) prohibiting the import of nursery stock and unmanufactured nonpropagative material (such as logs and mulch) 

of all oaks (Quercus), tanoak, Rhododendron spp., and evergreen huckleberry 

(Vaccinium ovatum Pursh) and of soil from areas where sudden oak death occurs. 

At about the same time, the California Board of Forestry declared an official Zone 

of Infestation for the seven counties (Santa Clara, Marin, Sonoma, Napa, Santa 

Cruz, San Mateo, Monterey) known to be infested with P. ramorum. The creation 

of the zone allowed for use of California Department of Forestry and Fire Protection resources to combat the problem. On May 17, 2001, the California Department 

of Food and Agriculture issued emergency regulations that restricted the export 

of diseased oak products and rhododendrons from the seven infested counties. 

The USDA Animal and Plant Health Inspection Service followed by issuing an 

interim federal regulation (7 CFR Part 301) on February 14, 2002, for domestic 

interstate movement of P. ramorum host materials from the seven infested California counties. In 2004, an emergency order expanded the regulated area to include 

nurseries in all of California, Oregon, and Washington. Internationally, regulations 

prohibiting import of potentially infested material were issued by Canada, Mexico, 

the European Union, the United Kingdom, the Czech Republic, Australia, New 

Zealand, South Korea, and Taiwan. By 2009, more than 68 countries, including 

China, either included P. ramorum on their lists of regulated pests or mentioned the 

pathogen in their legislation (Sansford and others 2009).

Following the first nursery findings in California in 2001, the pathogen was 

subsequently found in 20 nurseries in Oregon, Washington, and British Columbia. 

Movement of the pathogen in the nursery trade in North America and in Europe 
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GENERAL TECHNICAL REPORT PSW-GTR-234

became a major issue and concern. In 2004, P. ramorum was detected in two large 

southern California nurseries, and at one nursery in Oregon and one in Washington. 

It was subsequently determined by trace-back investigations that these nurseries 

had shipped potentially infected plants to over 1,200 nurseries in 39 states (Frankel 

2008). By 2005, a federal order was put in place (USDA APHIS 2007a) requiring 

that all nurseries in California, Oregon, and Washington that shipped host plant 

nursery stock interstate, be inspected and certified free of evidence of P. ramorum. 

Microsatellite marker techniques found that a single NA1 genotype (see chapter 2 

for discussion of P. ramorum genotypes) of the pathogen was shared among most 

states, and that isolates clustered into two genetic groups (one mainly containing 

isolates from Connecticut, Oregon, and Washington and the other group largely 

from California and the remaining states), suggesting two predominant eastward 

migration routes for NA1 individuals originating either in California or the Pacific 

Northwest (Goss and others 2010). 

In Europe

Because P. ramorum was known to be present in Germany and the Netherlands, 

surveillance for the pathogen in England and Wales began in July 2001, and later in 

other European countries (Brasier and others 2006a). The first finding of P. ramorum in the United Kingdom was confirmed in a nursery in April 2002 on Viburnum

tinus L. (Lane and others 2003). Phytophthora ramorum was subsequently found 

on southern red oak trees (Quercus falcata Michx.) in the United Kingdom, and on 

European beech (Fagus sylvatica L.) and American northern red oak (Q. rubra L.) 

in the Netherlands (Brasier and others 2004a). As in the United States, P. ramorum is known to have a wide and growing host range in Europe, affecting a large 

number of plant genera and species in the ornamental nursery trade, and in parks, 

gardens, and woodlands. Official controls currently include a ban on the import 

of susceptible host material from affected parts of the United States and plant 

passporting controls on the movement of Rhododendron, Viburnum, and Camellia within the European Union. Member States in the European Union are also 

required to conduct official surveys and to take action to prevent the spread of P. 

ramorum (Slawson and others 2006).

A complete chronology of important events in the P. ramorum story can be 

found on the COMTF Web site at http://nature.berkeley.edu/comtf/html/chronology.

html. The European Union risk analysis for the pathogen (Sansford and others 2009) 

provides information and references on the history of P. ramorum in the European 

Union and other European countries.
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

The Genus Phytophthora as Forest Pathogens

Phytophthora ramorum was not the first member of this genus to be a concern in 

forest ecosystems. The closest related species genetically, the apparently introduced 

pathogen P. lateralis, has resulted in significant damage to native forest ecosystems 

containing Port-Orford-cedar (Chamaecyparis lawsoniana (A. Murray) Parl.) in 

California and Oregon (Zobel and others 1985). The pathogen is significant because 

infection results in mortality of a host with a relatively limited distribution. The 

introduction of Phytophthora cinnamomi to the Southeastern United States in 

the early 1800s resulted in mortality of the American chestnut (Castanea dentata

(Marsh.) Borkh.) and related Castanea species (Crandall and others 1945, Mistretta 

1984) as well as being associated with littleleaf disease of shortleaf pine (Pinus 

echinata Mill.). The introduction of P. cinnamomi to eucalypt forests of Australia 

(Shearer and Smith 2000) and to oak forests of several Mexican states (AlvaradoRosales and others 2007, 2008; Tainter and others 2000) has resulted in similar 

drastic changes to forest ecosystems. 

Brasier (2003a) noted that pathogens in the genus Phytophthora became a major 

threat to European forests during the 1990s. During that decade, 12 previously 

unknown Phytophthora species were discovered in European forests or nurseries (Brasier 2003a). The ecological roles or places of origin of the species were 

unknown (Brasier 2003a). One species, P. alni, is of significant concern in Europe 

as the cause of alder dieback (Brazier 1999, Brasier and others 2004c, Gibbs and 

others 2003). Phytophthora alni is a hybrid species of complex parentage (Brasier 

and others 2004c, Ioos and others 2006). Recent surveys of streams and soils 

associated with alder stands in Alaska have found P. alni ssp. uniformis (Adams and 

others 2008). In the United Kingdom, the exotic species Phytophthora kernoviae 

has caused damage to beech and a range of other trees (Brasier and others 2005). 

Subsequent studies have isolated P. kernoviae from soils in indigenous and exotic 

forests in several regions of the North Island, New Zealand, and historical data 

indicate that it was first recorded in New Zealand (as Phytophthora sp.) in the 1950s 

(Ramsfield and others 2009).

In addition to the above examples of the genus Phytophthora as an introduced 

pathogen, recent investigations have found numerous species of the genus in 

forests of California and Oregon (Hansen 2003, Hansen and others 2006c, Rizzo 

and Fichtner 2009), in Eastern and Central U.S. oak forests (Balci and others 

2007, 2008), and in Europe (Brasier 1999, 2009; Brasier and others 1999). Hansen 

and others (2006c) discussed 15 distinct Phytophthora species from trees, soil, or 
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GENERAL TECHNICAL REPORT PSW-GTR-234

streams in oak forests in Oregon and California. In California and Oregon, two 

species, Phytophthora nemorosa and P. pseudosyringae, overlap in their host and 

geographic ranges with P. ramorum (Linzer and others 2009, Martin and Tooley 

2003), and symptoms on all hosts are indistinguishable from the symptoms caused 

by P. ramorum (Wickland and others 2008). The two species, along with 11 other 

species of Phytophthora, were found in a survey of ornamental nurseries in California (Yakabe and others 2009).

Brasier (2009) suggested that since the year 2000, 50 or more new species (species that have been morphologically and molecularly identified as unique although 

not yet necessarily formally described) of Phytophthora have been discovered. The 

ecological role and significance of these newly discovered species remains largely 

unknown.
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Chapter 2: Causal Agent, Distribution, 

Hosts, Diagnosis

The Causal Agent

The pathogen Phytophthora ramorum Werres, de Cock & Man in’t Veld was 

formally described in 2001 (Werres and others 2001). The previously undescribed 

species of Phytophthora had been observed since 1993 in Germany and the Netherlands associated with diseased rhododendron (Rhododendron), and since 1998 on 

diseased viburnum (Viburnum sp.). Pathogenicity to rhododendrons was demonstrated in 1997 (Werres and Marwitz 1997). 

Classification

Phytophthora ramorum belongs to the Kingdom Stramenopila (formerly in the 

Kingdom Chromista), a major eukaryotic group that includes diatoms and brown 

algae, and is distinct from plants, fungi, and animals. In contrast to fungi, stramenopiles are more closely related to plants than to animals. The taxonomy of P. 

ramorum (Alexopoulos and others 1996) is as follows:

Domain: Eukaryota

Kingdom: Stramenopila (Chromista)

Phylum: Heterokontophyta

Class: Oomycetes

Order: Peronosporales

Family: Pythiaceae

Genus: Phytophthora

Species Phytophthora ramorum

The Oomycetes, the class to which the genus Phytophthora belongs, share 

some superficial morphological and biological characteristics of fungi. Previous 

taxonomic classifications often placed these two groups together. However, they 

have since been found to be genetically distinct. Like fungi, Oomycetes exhibit 

filamentous growth, produce sexual and asexual spores, and can feed on decaying 

matter or be obligate parasites of plants. However, the nuclei within the Oomycete 

filaments are diploid, with two sets of genetic information, not haploid or dikaryotic as in fungi. Another difference is that fungal cell walls are made primarily of 

chitin, whereas Oomycete cell walls are constructed mostly of cellulose and glucan. 

In addition, Oomycetes have motile zoospores with two types of flagella, whereas 

most fungal spores have no flagella (Rossman and Palm 2006).
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GENERAL TECHNICAL REPORT PSW-GTR-234

Morphology

In culture, P. ramorum is characterized by the production of large, abundant 

chlamydospores and elongated, ellipsoidal, semi-papillate, deciduous sporangia. 

Hyaline chlamydospores (asexual survival structures) are produced on hyphal tips, 

becoming brown with age in culture and when produced on host tissue (Rizzo and 

others 2002b, Werres and others 2001). Chlamydospores are variously reported to 

range in size from 40 to 80 μm (Rizzo and others 2002b) and 20 to 91 μm (Werres 

and others 2001). The sporangia have a mean length of 43.6 μm (20 to 79 μm) and a 

mean width of 23.9 μm (12 to 40 μm) (Werres and Kaminski 2005). The heterothallic pathogen produces two mating types, A1 and A2. Oogonia with amphigynous 

antheridia are produced by pairings of opposite mating types (Brasier and Kirk 

2004, Werres and Kaminski 2005, Werres and others 2001). Oospores are not readily produced in culture, and no evidence of oospore formation has been reported in 

nurseries where both mating types have been present (Grünwald and others 2008a) 

or elsewhere in nature.

Genetic Diversity

Molecular analyses using microsatellite marker techniques indicate that populations 

of P. ramorum are clonal, consisting of three lineages (Grünwald and others 2008a, 

Ivors and others 2006b, Martin 2008). Characteristics of the three lineages are presented in table 1. The EU1 lineage is the only lineage found to date in Europe, with 

a few reports in nurseries in California, northern Oregon, Washington, and British Columbia, Canada (Garbelotto and others 2006, Grünwald and others 2008a, 

Hansen and others 2003). There has been one report of the EU1 lineage in forests 

in North America. The EU1 isolates, along with NA1 isolates, have been found in 

a woodland, coastal stream about 2 km from an infested nursery containing EU1 

isolates (but in a different watershed) in Humboldt County, California (COMTF 

2007). The NA1 is associated with infestations in California and Oregon forests, 

and also with a few nursery infestations in North America. The NA2 has a very 

Table 1—Nomenclature and characteristics of the known Phytophthora ramorum clonal lineages 

Clonal Current Mating Colony Colony Colony Aggressivelineage distribution Environment type type growth stability ness

EU1 Europe, Gardens, A1 Aerial Faster Stable Higher

 North America woodlands, 

 nurseries

NA1 North America Forests, nurseries A2 Appressed Slower Unstable Lower

NA2 North America Nurseries A2 Aerial Faster Stable Higher

Adapted from Grünwald and others 2008b, 2009; Sansford and others 2009.
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

limited distribution, being isolated to date from only a few nurseries in California 

and Washington State (Ivors and others 2006b). The NA2 lineage is distinctly 

different from EU1 and NA1; it behaves phenotypically like EU1 isolates but has 

a unique mitochondrial and microsatellite genotype. A Web site (http://people.

oregonstate.edu/~grunwaln/index.htm) hosted by Oregon State University provides 

information on multilocus microsatellite genotypes of P. ramorum currently found 

in North America.

All three lineages have occurred in U.S. nurseries, emphasizing the role of 

commercial plant trade in the movement of P. ramorum. Although sexual reproduction in nature has not been observed, the presence of isolates of both mating types 

at a single site might lead to genetic recombination, which could lead to an increase 

in pathogen fitness and host range.

In addition to differing in mating type, the clonal lineages differ in growth rate 

and colony type (Brasier 2003b, Brasier and others 2006b, Werres and Kaminski 

2005), aggressiveness (Brasier 2003b), nucleotide sequences in conserved genes 

(mitochondrial cytochrome c oxidase subunit 1) (Kroon and others 2004), and 

genetic diversity (Ivors and others 2004, 2006b). Isolates from the EU1 lineage are, 

on average, significantly more aggressive than isolates of the NA1 lineage isolates 

on Quercus rubra L. (Brasier 2003b, Brasier and others 2006b). EU1 isolates were 

more pathogenic than NA1 isolates on rhododendron (Pogoda and Werres 2002). 

Manter and others (2010) demonstrated that isolates belonging to clonal lineages 

EU1 and NA2 are generally more virulent, produce more sporangia, and produce 

more Ram-2 elicitin in vitro than do isolates belonging to lineage NA1.

Based on mitochondrial sequence analysis, Martin (2008) considered the EU1 

lineage to be basal to the NA1 lineage, and the NA2 lineage to be ancestral to both. 

Using DNA sequence variation analysis, Goss and others (2009a) did not observe 

DNA sequence variation differences among isolates within each lineage, suggesting that the genetic divergence among lineages preceded introduction. Analysis 

with coalescent-based methods revealed that the lineages have been diverged for 

an evolutionarily significant period of time, roughly 165,000 to 500,000 years. 

Genes contained signatures of historical recombination between the NA1 and EU1 

lineages, indicating that ancestors of the P. ramorum lineages reproduced sexually 

(Goss and others 2009a). 

Distribution

The native distribution or range of P. ramorum is not known. Evidence indicates 

that the pathogen has been separately introduced into North America and Europe 

from a third area, or areas, which are as yet undiscovered (Brasier 2003b, Ivors and 
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GENERAL TECHNICAL REPORT PSW-GTR-234

others 2004, Rizzo and others 2005). The divergence of the three clonal lineages 

of P. ramorum found by Goss and others (2009a) suggested to the authors that the 

three lineages originated from different geographic locations sufficiently isolated 

from each other to allow independent evolution prior to introduction to North 

America and Europe, and that the emergence of P. ramorum in North America and 

Europe was the result of three independent introductions.

The distribution of P. ramorum as an introduced nonnative species is now 

known to include the United States (specific nurseries in several states, and residential planting of infected stock from those nurseries in some cases; in wildlands only 

in Oregon and California) and Canada (nurseries only; under eradication) in North 

America, and several European countries (nurseries and limited outbreaks in parks 

and gardens/woodlands). See details provided below.

United States, in Forests 

Since the disease was first noted in 1995, the pathogen has been confirmed in natural settings, primarily redwood/tanoak and coastal evergreen forests, on various 

native hosts in 14 coastal California counties (Marin, Santa Cruz, Sonoma, Napa, 

San Mateo, Monterey, Santa Clara, Mendocino, Solano, Alameda, Contra Costa, 

San Francisco, Lake, and Humboldt), and in Curry County, Oregon. The infested 

California counties are contiguous and in central coastal California. Humboldt 

County is also coastal, and north of and contiguous with Mendocino County, but 

the known infestation in Humboldt is approximately 177 km north of any other 

California infestations, so it is relatively isolated. About 209 km separates the 

known locations in Humboldt County and Curry County in southern Oregon. See 

http://nature.berkeley.edu/comtf/html/maps.html for current distribution maps of the 

pathogen.

The pathogen was detected in 2001 via aerial survey in Curry County near 

Brookings, Oregon, just north of the California border where it was killing tanoak 

(Lithocarpus densiflorus (Hook. & Arn. (Rehd.) and infecting Pacific rhododendron 

(Rhododendron macrophyllum D. Don ex G. Don) and evergreen huckleberry 

(Vaccinium ovatum Pursh) (Goheen and others 2002a). At that time, nine infested 

forest sites totaling 16 ha were identified, and a 23-km2

 quarantine area was established around the area of infestation. Eradication treatments (cutting and burning 

all infected and nearby host plants as soon as possible after detection) from 2001 

through 2008 were completed on approximately 971 ha of forest at a cost of $4.3 

million (Kanaskie and others 2010a). 
13

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

United States, in Nurseries 

Phytophthora ramorum was first recovered from a nursery setting in the United 

States in 2001, when it was isolated from rhododendron container plants in a Santa 

Cruz nursery. In 2003, 20 additional nurseries were reported infested. In March 

2004, infestations of P. ramorum were detected in two large southern California 

nurseries. Those nurseries had shipped potentially infected plants to several thousand nurseries throughout most of the United States. Subsequently, 21 state and 

176 nursery-related detections were made (Garbelotto and Rizzo 2005). The large 

increase in number of positive nurseries in 2004 was due to the interstate shipments 

out of California and Oregon from infested nurseries and to a Federal Order requiring inspection for the first time of approximately 1,400 nurseries that ship host 

plants or associated plants in California, Oregon, and Washington (Jones 2006).

For January through September 2009, the U.S. Department of Agriculture, 

Animal and Plant Health Inspection Service (USDA APHIS) reported detection 

of P. ramorum in 11 states (California, Oregon, Washington, Alabama, Georgia, 

Maryland, Mississippi, New Jersey, North Carolina, Pennsylvania, South Carolina) 

at 30 sites: 24 nurseries and 6 in the landscape (Washington, Maryland, Pennsylvania, South Carolina) (http://www.aphis.usda.gov/plant_health/plant_pest_info/pram/

downloads/pdf_files/programupdate-2009-qtr3.pdf). All known infestations are 

apparently contained and under eradication (table 2).

Particularly noteworthy is the 2009 detection of P. ramorum on salal (Gaultheria shallon Pursh) in Pierce County, Washington. Water from a nearby infested 

nursery drains into the native forest containing salal. This is the first documented 

incident of the pathogen escaping from a nursery via runoff to infect native forest 

plants (COMTF 2009). 

Table 2—Detection of Phytophthora ramorum in U.S. nurseries by year

Year Number of Number of 

positive nurseries states

2000 (and prior) 0 0

2001 1 1 (California)

2002 0 0

2003 20 3 (California, Oregon, Washington)

2004 176 21

2005 99 7

2006 62 11

2007 23 6

2008 28 8

2009 (through 24 9 (plus landscape detections in four states)

 (September)
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GENERAL TECHNICAL REPORT PSW-GTR-234

Canada 

Phytophthora ramorum was first reported in Canada in June 2003, when infected 

potted rhododendrons were found in a British Columbia nursery (Sabaratnam and 

Woodske 2006). Additional detections occurred in 2004 and 2005 at a few nurseries and garden centers in British Columbia. Immediate regulatory action by the 

Canadian Food Inspection Agency (CFIA) has apparently successfully eradicated 

these occurrences. One nursery in Pitt River underwent a controlled burn followed 

by disinfection of soil and production areas in an attempt to eradicate the pathogen 

(Sabaratnam and Woodske 2006). In 2006, P. ramorum was detected at three retail 

garden centers that had been positive in 2004 (but negative in 2005), and eradication efforts continued at one wholesale nursery where P. ramorum was detected in 

late 2005 (NAPPO 2006). In 2007, the Canadian national survey for P. ramorum

found 10 positive nurseries in British Columbia; all were subject to eradication (Sela 

2008). See (http://www.inspection.gc.ca/english/plaveg/pestrava/phyram/sodmsce.

shtml) for survey results in Canada.

Europe

Since the first reports in Germany and the Netherlands (Werres and others 2001), 

P. ramorum has been discovered in additional European countries. In the European 

Union, P. ramorum has been recorded as present in Belgium, Czech Republic 

(eradicated nursery finding), Denmark, Estonia, Finland, France, Germany, Ireland, 

Italy, Latvia, Lithuania, Luxembourg, the Netherlands, Poland, Portugal, Slovenia, 

Spain (including Mallorca), Sweden, and all the United Kingdom (U.K.) countries, 

including the Channel Islands. Additional European countries where P. ramorum

has been recorded include Norway and Switzerland (Delatour and others 2002, 

De Merlier and others 2003, Heiniger and others 2004, Herrero and others 2006, 

Lane and others 2003a, Lilja 2007, Moralejo and Werres 2002, Orlikowski and 

Szkuta 2002, Orlikowski and others 2004) and Serbia (Bulajić and others 2009). 

The pathogen was found in the Czech Republic on imported Viburnum plants 

in 2003, but this outbreak was considered eradicated as further surveys in 2004 

and 2005 did not detect the pathogen (Běhalová 2006) (http://www.forestry.gov.

uk/pramorum). In these European countries, the pathogen is mainly present on 

nontree hosts grown in containers at nurseries and retail garden centers. However, 

in Belgium, Denmark, France, Germany, Ireland, Luxembourg, the Netherlands, 

Slovenia, Spain, the United Kingdom, as well as the non-EU countries of Norway, 

Switzerland, and Serbia, some infected plants have been found outside nursery situations in managed parks and gardens and in woodland situations (Bulajić and others 

2009, Sansford and others 2009). 
15

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

In Europe, infected trees with P. ramorum bole cankers have only been found 

in the United Kingdom and the Netherlands (Brasier and others 2004b, Denman 

and others 2005a, Gewasbescherming 2004, Mycological Research News 2004, 

Sansford and others 2009). In November 2003, the first P. ramorum-infected tree 

outside the United States was confirmed on a mature (100-year-old) southern red 

oak (Quercus falcata Michx.) tree in Sussex, United Kingdom. Infection of several 

Quercus rubra trees in the Netherlands was confirmed about the same time. By 

2007, a range of tree species in Cornwall, United Kingdom—especially beech 

(Fagus sylvatica L.) but also including turkey oak (Q. cerris L.), sessile oak (Q. 

petraea (Matt.) Liebl.), Q. falcata, evergreen oak (Q. acuta Thunb.), horse chestnut 

(Aesculus hippocastanum L.), sweet chestnut (Castanea sativa Mill.), roble beech 

(Nothofagus obliqua (Birb.) Blume), sycamore (Acer pseudoplatanus L.), and a 

species of Schima—had been found with bleeding bark cankers. Other trees have 

been found with only foliar or dieback symptoms, for example holm oak (Quercus 

ilex L.), castanopsis (Castanopsis sp.), camphor tree (Cinnamomum camphora

(L.) J. Presl), ash (Fraxinus excelsior L.), Michelia doltsopa Buch.-Ham. ex DC., 

winter’s bark (Drimys winteri Forsr.), evergreen maple (Acer laevigatum Wallich), 

Cornus kousa Hance x capitata Wall. ex Roxb., an unconfirmed species of Eucalyptus, Delavay osmanthus (Osmanthus delavayi Franch.) and Chinese guger tree 

(Schima wallichii (DC.) Korth.) as well as several species of Magnolia L. (Sansford 

and Woodhall 2007). Some tree hosts in Europe can exhibit both foliar and bole 

infections, e.g., turkey oak and sweet chestnut. Japanese larch (Larix kaempferi

(Lam.) Carrière) was found as both a bole host and foliar (sporulating) host in 

Devon, Cornwall, and Somerset, southwest England, in 2009 (Forestry Commission 

2009). Symptoms have also been found on western hemlock (Tsuga heterophylla

(Raf.) Sarg.) and broadleaf species (beech [Fagus spp.], birch [Betula spp.], and 

some oaks) growing in the same area (Forestry Commission 2009). Infected 

rhododendrons (especially the invasive R. ponticum L.) have been in proximity to 

most bleeding canker infections on infected U.K. and Netherlands trees (Sansford 

and Woodhall 2007). Rhododendrons are not associated with many of the infected 

Japanese larch and western hemlock.

Hosts

Phytophthora ramorum is a generalist pathogen with a broad and diverse host range 

that continues to expand. The host list includes both hardwood and conifer trees, 

shrubs, herbaceous plants, and ferns. Some hosts are found in forest situations, 

whereas others are used widely as landscape and ornamental plants. In coastal 

California forests, P. ramorum infects many different plant species, and in some 
16

GENERAL TECHNICAL REPORT PSW-GTR-234

mixed-evergreen forests nearly all woody plants can serve as hosts for P. ramorum

(Rizzo and others 2002a). 

Plant species are designated as regulated hosts and as associated plants by the 

U.S. Department of Agriculture (USDA). The difference between hosts and associated plants is the demonstration of Koch’s postulates (criteria designed to confirm 

that a micro-organism associated with symptoms of a disease is the cause of the 

disease). Proven or regulated hosts are hosts for which Koch’s postulates have been 

completed, documented, reviewed, and accepted to confirm they are host plants of 

P. ramorum. All host parts, except the wood of non-bole hosts, are regulated (see P. 

ramorum quarantine and regulations at http://nature.berkeley.edu/comtf/pdf/APHIS2005-0102-0001.pdf). 

Associated plants are plants that have been found to be naturally infected 

with P. ramorum, and P. ramorum has been cultured and/or detected using polymerase chain reaction (PCR), but Koch’s postulates have not been completed or 

documented and reviewed, and for which testing has not been completed. Taxa 

are moved from the Associated Plant List to the Regulated Host List when Koch’s 

postulates are demonstrated and reviewed (Cave and others 2005). USDA APHISPlant Protection and Quarantine (PPQ) maintains an updated list of regulated and 

associated hosts at http://www.aphis.usda.gov/plant_health/plant_pest_info/pram/

downloads/pdf_files/usdaprlist.pdf.

As of May 2008, the list contained 45 regulated hosts and 72 associated plants 

that are regulated as nursery stock. A list of natural hosts of P. ramorum in the 

United Kingdom, Europe, and North America is available in the 2009 European 

pest risk analysis for P. ramorum (Sansford and others 2009). The list includes the 

location of the finding (the United Kingdom, other European countries, Canada, the 

United States), symptoms, and literature reference.

A third category, experimental hosts, also exists. Experimental hosts, in contrast to the above two previously described groups where the pathogen is found 

on naturally infected plants, are those for which pathogenicity was determined by 

inoculating various plants to predict potential hosts. If the plant becomes infected, 

it is not added to the hosts or associated plants lists unless found naturally infected. 

More than an additional 40 plant genera have been susceptible to this pathogen in 

inoculation trials. Some of the literature that screened for potential hosts includes 

Brasier and others (2002), Chastagner and others (2006b), Denman and others 

(2005b), Hansen and others (2005), Parke and others (2002a), Rizzo and others 

(2002a), Tooley and Kyde (2003, 2007), and Tooley and others (2004). The European risk analysis (Sansford and others 2009) contains a table of the experimental 

host range (susceptible species determined experimentally) and references.
17

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

The California Oak Mortality Task Force (COMTF) Web site (www.

suddenoakdeath.org) contains the most up-to-date information available on regulated hosts, associated plants, and experimental hosts. See http://nature.berkeley.

edu/comtf/html/host_plant_lists.html#AssociatedHosts for lists of regulated and 

associated hosts. Also see the host lists maintained by RAPRA (risk analysis for 

Phytophthora ramorum) at http://rapra.csl.gov.uk/. Because the lists are being constantly updated, the Web sites and others should be checked for the latest information on hosts.

Symptoms

Three different diseases—stem or bole canker, twig blight (dieback) and leaf 

blight—are attributed to P. ramorum (Hansen and others 2002): “sudden oak 

death” in the United States, also known in Europe as “ramorum bleeding canker,” 

characterized by bleeding bark cankers on the bole, which can be lethal; “ramorum 

shoot dieback,” resulting from foliar infection or infection of stems; and “ramorum 

leaf blight,” resulting from foliar infection. Thus, the symptoms produced by P. 

ramorum are diverse and range from trunk and branch cankers to foliar symptoms 

including leaf spots, leaf lesions, leaf/twig/stem blights, depending on the host plant 

and the part of the host affected. Individual plant species can display more than 

one disease type (for example, leaf blight, shoot dieback, and bleeding cankers on 

tanoak). A comparison of symptoms of sudden oak death and ramorum blight (a 

combination of shoot dieback and leaf blight) is presented in table 3.

The COMTF Web site (http://nature.berkeley.edu/comtf/html/plant_symptoms.

html) contains descriptions and images of symptoms. Several diagnostic guides 

are available at that site with descriptions and pictures of symptoms on many host 

plants (Davidson and others 2003b, Storer and others 2002). 

Table 3—Comparison of sudden oak death and ramorum blight caused by Phytophthora ramorum

Host Geography/

Disease Symptoms categories Typical hosts environment

Sudden oak death Stem cankers; Forest and Coast live oak, North American 

 bleeding cankers garden trees tanoak, European forests, European

 beech, others gardens

Ramorum blight Foliar and twig Ornamental trees California bay 

 blight; tip and and woody shrubs; laurel, North American 

 shoot dieback; understory plants rhododendron, nurseries and

 leaf blight Viburnum, Pieris, forests, European

 coast redwood, nurseries and

 tanoak, others gardens

Modified from Grünwald and others 2008b.
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GENERAL TECHNICAL REPORT PSW-GTR-234

Disease symptoms are reviewed and well-illustrated in many other publications including Garbelotto and others 2002a; McPherson and others 2002a; Parke 

and others 2003, 2004; Storer and others 2002; and Tjosvold and others 2005. 

McPherson and others (2002a) included descriptions of symptoms by host family. 

The RAPRA Web site (http://rapra.csl.gov.uk/background/hosts.cfm) contains links 

to images of symptoms on various hosts. 

Phytophthora ramorum has been isolated from asymptomatic host tissue, 

including asymptomatic root tissue of infected tanoak seedlings (Parke and others 

2006b); asymptomatic stems and roots of Rhododendron spp. (Bienapfl and others 

2005); and leaves of Rhododendron “Cunningham’s White” and holm oak (Quercus 

ilex) being used as trap plants (Denman and others 2009). 

Similar-Looking Diseases

Signs and symptoms produced by P. ramorum are variable, not unique, and often 

indistinguishable from those caused by other plant pathogens (including other 

Phytophthora species), insect problems, abiotic or physiological conditions, and 

injuries. The presence of the pathogen can only be confirmed through laboratory 

diagnosis using species-specific diagnostic methods (for example, by isolation of the 

pathogen onto agar media, or by molecular tests). 

Look-alike diseases, insect damage, or other injuries or conditions are 

described and illustrated in numerous publications. Some of the most comprehensive for oaks and tanoak include descriptions on the COMTF Web site (http://

nature.berkeley.edu/comtf/html/look-alikes_misdiagnosis.html), the Forest Service 

Western and Eastern Pest Alerts (Frankel 2002, O’Brien and others 2002), and the 

University of California Pest Alert Number 6 (Storer and others 2002). 

Diagnostics

For reasons stated above, diagnosis of P. ramorum based on symptoms alone 

is unreliable. Methods for detecting plant pathogens in host tissue—plating on 

selective media (isolation and culture), and molecular techniques/assays based on 

either proteins (Enzyme-linked immunosorbent assay [ELISA]) or DNA (methods 

based on the polymerase chain reaction [PCR])—have been used for P. ramorum. 

Culturing or molecular diagnostics are necessary for confident identification of P. 

ramorum.

Plating on Selective Media (Isolation and Culture) 

Traditional isolation techniques used for other Phytophthora species are successful 

for recovery of P. ramorum from tissue of many host species. Plating host material 
19

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

taken from the leading edge of a canker or lesion onto semiselective media for 

Phytophthora, such as pimaricin-ampicillin-rifampicin-pentachloronitrobenzene 

(PARP) (Erwin and Ribeiro 1996), incubating the plates in the dark at 20 to 22 

°C, and examining within 2 to 5 days has been commonly used (Davidson and 

others 2003b). Once P. ramorum is growing in culture, its identity is confirmed by 

microscopic examination for its unique morphological characteristics or by speciesspecific molecular tests (see below). The USDA APHIS-PPQ protocol for cultural 

isolation is found at http://www.aphis.usda.gov/plant_health/plant_pest_info/pram/

downloads/pdf_files/cultureprotocol6-07.pdf . A diagnostic protocol developed by 

the European and Mediterranean Plant Protection Organization (EPPO) is available 

at http://www.furs.si/law/eppo/zvr/ENG/EPPO2004/diag_protokoli_PM7/pm7-66.pdf.

Although traditional isolation-based diagnostics are successful, there are several associated issues. Culturing of the pathogen from symptomatic plant material 

is time consuming, and under some circumstances, its success may be dependent 

on the species of the host or the environmental conditions from which the sample 

was taken (Martin and others 2004). Isolation success is extremely variable based 

on plant substrate and time of year (Davidson and others 2005b, Garbelotto 2003b). 

The fungicides and antibiotics in the selective media may sometimes suppress 

the development of hyphae from plant tissue or the development of Phytophthora

propagules (Davidson and others 2003b). Furthermore, despite P. ramorum's 

distinctive morphological characteristics, closely related Phytophthora species can 

have overlapping morphology characters, and the identification of an unknown 

culture solely on the basis of morphology requires training and experience. Because 

of these limitations, molecular diagnostic approaches have been developed and are 

used to augment detection and identification of the pathogen.

Serological Methods

The ELISA technique (Gaastra 1984) is a serological test used to detect the presence or absence of specific antigenic proteins produced by all Phytophthora species. 

If a large number of samples are to be processed for P. ramorum, ELISA is used as 

a low-cost, prescreen to reduce the number of samples that will need to be processed for subsequent tests. An ELISA test that is specific to P. ramorum is not yet 

available.

ELISA tests are available in packaged kit form. Single-test, self-contained 

ELISA kits are commercially available for laboratory use; the one produced by 

Agdia Inc. (Elkhart, Indiana) is approved by APHIS. Another kit, developed in the 

United Kingdom and marketed as a “lateral flow device” (LFD), principally for infield use, by Forsite Diagnostics Ltd., York, for Phytophthora species, was evaluated 
20

GENERAL TECHNICAL REPORT PSW-GTR-234

by Lane and others (2007). Although false positives were common, their assay was 

simple to use, and provided results comparable to laboratory methods (isolation and 

real-time PCR) in a few minutes. Results suggested that the use of LFD at the time 

of inspection may be a useful primary screen for selecting samples for subsequent 

laboratory testing to determine species. Avila and others (2010) reported development of antibodies that, when used in ELISA, recognized P. ramorum and P. 

kernoviae, detected a smaller spectrum of other Phytophthora species, and did not 

cross react with Pythium species.

For making regulatory determinations, USDA APHIS-PPQ encourages the use 

of a procedure that incorporates Agdia’s ELISA test for screening of all samples 

(http://www.aphis.usda.gov/plant_health/plant_pest_info/pram/downloads/

pdf_files/ELISA.pdf ). The procedures used by the USDA to determine the presence or absence of P. ramorum in plant samples, summarized by Berger (Berger 

2006), is based on a combination of tests. The Agdia-based ELISA is encouraged 

so that further screening on Phytophthora-negative samples is avoided. ELISA 

negative samples are considered negative for P. ramorum by the USDA. Samples 

that are positive on the basis of ELISA are then subjected to further testing using 

DNA-based techniques. Laboratories have the option, either before or after ELISA 

testing, to try to culture the organism. Presumptive positive cultures are then sent 

to the National Mycologist in Beltsville, Maryland, for confirmation. If cultural 

isolation is confirmed, the sample is considered positive, even in rare cases where 

PCR (if done) is negative. For samples that are ELISA positive, but from which P. 

ramorum was not isolated, or that are ELISA positive and no culture was attempted, 

DNA is extracted and the DNA sent to the National Identification Service (NIS) 

(Beltsville, Maryland), for PCR analysis.

The complete and rather involved details of the APHIS-PPQ system for sample 

submission from provisionally approved laboratories, referred to as the “Potentially 

Actionable Suspect System” (PASS), are available at http://www.aphis.usda.gov/

plant_health/plant_pest_info/pram/downloads/pdf_files/passpolicy_mar08.pdf. 

DNA-based Techniques/Assays

Several DNA-based molecular techniques (among others, PCR of the ITS region 

or other regions of the genome, real-time PCR, amplified fragment length polymorphism (AFLP), inter simple sequence repeat (ISSR), microsatellites, sequence 

analysis of several genes and PCR-restriction fragment length polymorphism 

[RFLP]) have been developed for detection and characterization of P. ramorum

(Bonants and others 2006, Kox and others 2007). 
21

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

PCR—

Amplifying unique DNA sequences, such as the internal transcribed spacer (ITS) 

region, by using species-specific primers, has been used as a method for screening 

of other Phytophthora spp. (Bonants and others 1997, Cooke and others 2000b, 

Kong and others 2003b). Because the ITS region is conserved across Phytophthora

spp. but differs among species within the genus, and the ITS sequence in that region 

is known for most Phytophthora spp. (Cooke and others 2000a, 2000b; Lee and 

Taylor 1992), ITS PCR has been used successfully for detection of specific Phytophthora species.

Based upon ITS sequence analysis, a species-specific PCR detection method 

for P. ramorum was developed and validated using stem and leaf material from 

plants infected with P. ramorum (Garbelotto and others 2002b, Kox and others 

2002). The primers developed may show cross reaction with P. lateralis (Kox and 

others 2002) and with P. cambivora at high concentrations (Davidson and others 

2003b). Primers developed by K. Hughes (Lane and others 2003a) are specific to 

P. ramorum. A PCR-based molecular diagnostic assay initially developed for P. 

lateralis (Winton and Hansen 2001) is also effective for P. ramorum, and remains 

the primary molecular diagnostic test used in Oregon for diagnosis of P. ramorum

from the forest. 

Nested PCR may be required to detect low levels of infection when small 

amounts of the pathogen are present (Bonants and others 1997, Gunderson and 

others 1996, Hayden and others 2004, Martin and others 2004). Nested PCR is 

basically the same as regular ITS PCR using species-specific primers, but the PCR 

reaction is run twice, with different combinations of primers. The test is thus able 

to detect much smaller amounts of DNA in a sample. However, nested PCR is much 

more prone to false positives resulting from laboratory contamination and other 

factors, including the presence of inhibitors. To be used with confidence, it requires 

dedicated laboratories with strict procedures and numerous internal controls. In 

a comparison between successful diagnoses in California forests using a nested 

PCR approach and traditional isolation techniques, nested PCR showed the greater 

sensitivity (Hayden and others 2004). However, PCR was not always successful in 

detecting the pathogen and was highly dependent on which plant part (for example, 

wood vs. leaves) or plant species was tested (Hayden and others 2004). The most 

promising results in forest surveys were obtained from traditional isolation combined with ITS PCR-based assays (Hayden and others 2004).

Real-time PCR assays, especially those based on TaqMan chemistry (Holland 

and others 1991), are increasingly preferred to gel-based PCR. They are quicker, 
22

GENERAL TECHNICAL REPORT PSW-GTR-234

less labor-intensive, and are less prone to post-PCR contamination because subsequent manipulation of amplified DNA is avoided (Schaad and Frederick 2002). 

A nested real-time PCR assay, based on SYBR®-Green technology, was 

developed by Hayden and others (2004). These authors (Hayden and others 2004) 

developed and tested a real-time, nested PCR assay that was sensitive and hostspecific for P. ramorum. The technique allowed the confirmation of P. ramorum in 

symptomatic plants and facilitated the expansion of the host range by 10 hosts and 

four California counties far sooner than if identification had been based on pathogen isolation alone. 

A real-time quantitative PCR method that measures PCR product accumulation 

through a dual-labeled fluorogenic probe (TaqMan® probe) was developed in 1996 

(Heid and others 1996). Real-time PCR methods based on TaqMan chemistry do 

not require certain pre-amplification steps and therefore reduce the risk of crosscontamination. A TaqMan probe has been developed for P. ramorum based upon 

the ITS sequence (Ivors and Garbelotto 2002). 

Hayden and others (2006) developed and tested a nested TaqMan assay that 

included a first-round amplification step. The assay was as sensitive as the real-time 

PCR assay developed by Hayden and others (2004) that used SYBR-Green for 

detection. The nested TaqMan method successfully detected P. ramorum in fieldcollected samples (Hayden and others 2006). Sensitivity of the assay was markedly 

increased with the nested protocol vs. single-round, with detection rates more than 

doubled (Hayden and others 2006). Their technique provided for both detection and 

quantification of P. ramorum in plant material, even in the presence of inhibitors 

and low concentrations of P. ramorum DNA. However, because the assay requires 

two reactions and the moving of the product to a new tube, it has a risk of contamination.

When comparing isolation of P. ramorum using PARPH medium (cultural 

isolation using a variation of the PARP medium previously described) with a 

real-time PCR TaqMan assay developed by the Central Science Laboratory (York, 

United Kingdom), the two techniques were equally reliable and robust for diagnosis 

of P. ramorum from the U.K. plant material tested (Hughes and others 2006a). 

A single-round, real-time TaqMan PCR assay for the detection of P. ramorum, 

involving no post-amplification steps or nested PCR, has been developed (Hughes 

and others 2006c). The single-step protocol eliminates possible contamination 

introduced between the first and second round of PCR when using nested PCR. 

The assay detected P. ramorum in plant material containing as little as 1 percent 

infected material by weight. The real-time protocol gave results comparable with a 

traditional isolation technique for diagnosis of P. ramorum in plant material from 
23

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

common U.K. hosts (Hughes and others 2006c). This assay is routinely used at the 

Central Science Laboratory in the United Kingdom, in conjunction with isolation 

techniques, for the detection of P. ramorum in symptomatic plant material in the 

laboratory.

Amplification of more than one region of DNA simultaneously (multiplex PCR) 

was first used as a diagnostic test for Phytophthora by Winton and Hansen (2001). 

Their technique amplifies a very highly conserved region of DNA as well as the 

piece of ITS DNA specific to Phytophthora lateralis and P. ramorum, resulting in 

a built-in check on the reaction (if the conserved region, found in all living organisms, does not amplify, then something is wrong with the test). Multiplex PCR, 

which can be used for simultaneous (multiplex) detection of more than one pathogen 

species in a sample of plant tissue and is a next step from single-species detection, 

provides benefits to programs such as national surveys where large numbers of samples are involved. In addition, multiplex PCR can be used to incorporate a variety of 

control reactions to measure the quantity and integrity of the DNA tested. Various 

modifications of existing TaqMan assays and other new approaches are being 

developed for parallel testing. For example, Tooley and others (2006) used a realtime PCR method based on TaqMan in a three-multiplex format to simultaneously 

detect P. ramorum, P. pseudosyringae, and plant DNA in a single tube. Schena and 

others (2006) developed a real-time multiplex PCR assay based on TaqMan PCR to 

simultaneously identify and detect P. ramorum, P. kernoviae, P. quercina, and P. 

citricola within the same plant extract.

Bilodeau and others (2009) developed two multiplex real-time PCR assays 

using TaqMan probes with different reporter dyes targeting P. ramorum (ITS), 

Phytophthora genus (β-tubulin), oomycetes (ribosomal 5.8S subunit), and host 

plants (RuBisCO). This allowed simultaneous detection of P. ramorum while 

verifying DNA extraction and the presence of other oomycetes in the DNA sample. 

The multiplex assays detected P. ramorum accurately while decreasing the cost 

and increasing throughput. The advantage of the multiplex assays is that the presence of an internal control should reduce the rates of false negatives by identifying 

reactions that failed owing to poor DNA extraction or to the presence of inhibitors 

(Bilodeau and others 2009).

Fingerprinting or barcoding methods—

Single-strand conformation polymorphism (SSCP) analysis is an effective molecular fingerprinting technique for species differentiation in the genus Phytophthora, 

and P. ramorum shows a unique pattern of ribosomal DNA ITS 1 when analyzed 

(Kong and others 2003b, 2003c, 2004). The SCCP procedure separates species 
24

GENERAL TECHNICAL REPORT PSW-GTR-234

based on the PCR-amplified ITS DNA sequence, but indirectly. Differences in 

sequence between species cause the strands of DNA to assume different shapes 

(conformations) and thus to move at different speeds through an electrophoresis gel. 

The SSCP analysis reported by Kong and others (2004) was rapid and efficient, and 

SSCP profiles easily distinguished P. ramorum from other described Phytophthora

species. The authors suggested that SSCP analysis may be a superior technique to 

other existing molecular fingerprinting methods such as restriction fragment length 

polymorphism (RFLP). However, because each Phytophthora species is identified 

by a profile of three bands, presence of multiple species in the same sample may 

be confusing; in addition, SSCP from environmental rather than cultural samples 

may result in spurious bands (Garbelotto 2003b). A modification of the technique 

using fluorescent-labeling chemistry and an additional marker locus was successfully used to allow quantitative matching of Phytophthora isolates from streams, 

soil, and plants with reference species (Hansen and others 2006a). Kong and others 

(2006) reported a modification of their 2003 (Kong and others 2003c) technique that 

provided reliable diagnoses of P. ramorum, whether it is a single infection or dual 

infection (a second Phytophthora species involved). The technique also provided 

accurate diagnoses of diseases caused by 12 other species of Phytophthora without 

additional work.

Microsatellite techniques and amplified fragment length polymorphism (AFLP) 

have been successfully used to differentiate between the North American and European lineages of P. ramorum (Hansen and others 2003). An AFLP DNA fingerprinting showed significant differences between EU and U.S. populations (Bonants 

and others 2002, Ivors and others 2002). Using sequence differences between EU 

and U.S. isolates of P. ramorum in the mitochondrial cytochrome c oxidase subunit 

1 (cox1) gene, Kroon and others (2004) developed a single-nucleotide polymorphism (SNP) protocol to distinguish between isolates of P. ramorum originating in 

Europe and those originating in the United States. All isolates could be consistently 

and correctly allocated to either the European or the U.S. populations using the 

SNP protocol. Whereas European isolates of P. ramorum shared a unique RFLP 

profile, U.S. isolates had a different RFLP profile similar to that of P. brassicae. 

However, P. brassicae showed additional fragments and was distinguishable from 

P. ramorum isolates (Kroon and others 2004). Elliott and others (2009) developed 

techniques to identify P. ramorum isolates according to each of the three lineages 

using PCR-RFLP of the cox1 gene.

Microsatellite analysis of P. ramorum was first developed in the Hansen lab at 

Oregon State University. Large numbers of P. ramorum isolates have been analyzed 

with AFLP (Ivors and others 2004). Results show two clusters, with EU isolates 
25

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

and U.S. isolates grouping separately. Using the recently assembled whole-genome 

sequence of P. ramorum, simple sequence repeat (SSR) techniques were used to 

fingerprint large numbers of P. ramorum isolates originating from different host 

species within Europe and the United States (Ivors and others 2006a). Many loci 

showed variation between the EU and U.S. populations. Minor variation was found 

within the EU populations and even less variation within the U.S. population. 

Onsite real-time PCR techniques—

Tests that can be reliably used immediately at the point of sampling rather than 

requiring one to send samples to a central laboratory for testing and to wait for 

results would be useful in certain instances. For example, availability of onsite 

testing techniques would permit the targeted testing of known P. ramorum hosts, 

such as imported nursery stock, at points of entry with minimal disruption to trade. 

In addition, onsite testing would reduce the need to hold suspect material while 

waiting for a laboratory test result. If an onsite test is suitably sensitive, samples that 

test positive in the field can then be sent to a diagnostic laboratory for confirmation. 

Because the current methods for the molecular detection of fungal pathogens in 

plant material require the extraction of DNA (Schaad and Frederick 2002), onsite 

molecular testing requires a portable real-time PCR platform and a suitable assay, 

as well as a simple and robust method for extracting DNA in the field.

Tomlinson and others (2005) developed a rapid and simple method for DNA 

extraction from symptomatic foliage and stems in the field, followed by a real-time 

PCR (TaqMan) assay using a portable real-time PCR platform (Cepheid SmartCycler II) for accurate onsite detection of P. ramorum within 2 hours. The combination of an extraction method, real-time PCR assay, and lyophilized, field-stable 

reagents, all optimized for use in the field, allowed the detection of P. ramorum

in naturally infected material at the point of sampling, with results comparable to 

those of real-time PCR testing in the laboratory. A variation of that method was 

successfully evaluated under U.S. conditions using leaf and stem samples from 20 

plant species collected from five sites around San Francisco, California (Hughes 

and others 2006b).

Tomlinson and others (2007) developed a number of assays based on their 

earlier method (Tomlinson and others 2005) that had various advantages for use in 

the field. A variation of a real-time PCR assay called “scorpion runs,” was twice as 

fast as TaqMan, and allowed the detection of P. ramorum in less than 30 minutes. 

They also designed a loop-mediated isothermal amplification (LAMP) assay, which 

allowed sensitive and specific detection of P. ramorum (as indicated by a color 

change visible to the naked eye) in 45 minutes using only a heated block to maintain 

a single constant temperature.
26

GENERAL TECHNICAL REPORT PSW-GTR-234

Riedel and others (2010) are developing a stationary PCR chip with integrated 

microstructured heaters and temperature sensors for the amplification of specific 

Phytophthora DNA fragments. A microfluidic system connects the PCR chip with 

a microarray where the labelled DNA fragments are detected. The miniaturization 

of the chip-formatted PCR and array system enables high portability, low input of 

energy, smaller amounts of expensive analytic chemicals, and very fast reaction 

times owing to low reaction volumes.

APHIS PPQ Protocol

The current (as of June 5, 2007) diagnostic protocol used by APHIS PPQ (USDA 

APHIS 2007b) for samples that have regulatory significance states that all samples 

that are ELISA positive and/or culture negative must be assayed using the validated 

nested PCR method by USDA or at authorized USDA laboratories. The DNA is 

extracted from ELISA positive samples (see http://www.aphis.usda.gov/plant_

health/plant_pest_info/pram/downloads/pdf_files/pcrprotocol4.pdf ), and these 

DNA extracts are forwarded to the National Identification Services (NIS) Molecular 

Diagnostic Lab (which at present is the only authorized laboratory) as described 

in the protocol. If the diagnostic laboratory has not performed the ELISA test, 

then culture negative samples need to have DNA extracted and these extracts sent 

to the NIS Molecular Diagnostic Lab for analysis. Several labs outside of USDA 

authorized labs have been provisionally approved to process diagnostic samples 

using the USDA validated protocols. For the majority of regulatory samples, these 

labs provide final determinations. Only potentially actionable suspect samples 

need to be forwarded for USDA confirmation. This laboratory approval program 

has several quality assurance measures in place to ensure participating laboratory 

capabilities and proficiency. 

The APHIS PPQ protocol utilizes two PCR tests for P. ramorum determination 

(Berger 2006). The first is the multiplex PCR developed by Oregon State University (OSU) (Winton and Hansen 2001). Although it is not as sensitive as the main 

diagnostic test and can produce false positive results with a few other closely related 

Phytophthora species, the OSU test is used as a quality assurance procedure to 

ensure that DNA received by PPQ is of sufficient quantity and quality to be amplifiable in the nested PCR test. Any DNA samples that do not meet these criteria are 

not tested further, and a new sample is requested. The second assay, assuming that 

amplifiable DNA is present in the sample, is a validated nested PCR test, modified 

slightly from the technique developed at the University of California at Berkeley, 

and described in http://www.aphis.usda.gov/plant_health/plant_pest_info/pram/

downloads/pdf_files/pcrprotocol4.pdf. Any sample DNA that passed amplification 
27

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

quality control, and that reacted to produce either a nested PCR or a Phytophthoraspecific multiplex PCR product, or both PCR products, is retested using both 

conventional PCR assays, and is tested in the real-time PCR assay. Results of different replications of assays on individual samples are compared to confirm that the 

results were both repeatable, and robust. If the results of different replications of the 

assays for any sample are not all conclusive and compatible, DNA sequences are 

obtained for conventional PCR products, and these sequences are compared to those 

of reference sequences contained in public and local databases to aid in completing 

a diagnosis. Although a rare occurrence, if a diagnosis cannot then be obtained, a 

new sample is requested (Berger 2008).

APHIS also has validated an additional real-time PCR assay for P. ramorum. 

This test is based on the test currently used in the United Kingdom and developed 

by the Central Science Laboratory (York, United Kingdom). It is robust and sensitive, incorporates DNA quality controls into the single reaction, and has higher 

throughput than current APHIS methods. Comparative analysis with the primary 

PCR diagnostic demonstrated that this real-time PCR protocol is less sensitive than 

the original test, so some samples that cannot be confirmed with this test because of 

low concentration of P. ramorum need additional testing for confirmation. Recent 

research has provided a comparative analysis to determine the correlation among 

ELISA, culture, real-time, and conventional PCR detection and is described below 

(Bulluck and others 2006). In addition, collaborative work involving several U.S., 

Canadian, and U.K. laboratories has occurred to help identify the most promising 

tests for entrance into the validation process.

EPPO Protocol

The European and Mediterranean Plant Protection Organization (EPPO) publishes 

standards on diagnostic protocols for regulated pests of the EPPO region, including the European Union. The provisional diagnostics protocol for P. ramorum, 

approved September 2005, was published as PM (phytosanitary measures) 7/66(1) 

in 2006 (OEPP/EPPO 2006). The publication contains a summary of sampling 

procedures for plants, water, and soil; methods for isolation from plants, water, and 

soil; and a section on identification of the pathogen, including growth and morphology in culture, biochemical methods, and molecular methods. Web link (via 

EPPO Web site): http://www3.interscience.wiley.com/cgi-bin/fulltext/118562438/

PDFSTART. 

Relative Sensitivity and Specificity of Diagnostic Techniques

In addition to those already mentioned, several research efforts designed to obtain 

information on the relative sensitivity and specificity of the diagnostic tests used for 
28

GENERAL TECHNICAL REPORT PSW-GTR-234

P. ramorum identification—including culturing, ELISA, nested PCR, and real-time 

PCR—have been conducted or are underway. 

In a comparison of diagnostic techniques within a nursery setting (Bulluck 

and others 2006), a block of 300 camellia (Camellia spp.) plants within a California 

nursery known to be infested with P. ramorum was simultaneously assayed for 

visual symptoms, growth medium pH, and moss presence. Host plant leaf tissue or 

leaf bait from the growth medium extracts were either plated on PARP-V8, tested 

using ELISA, or subjected to either nested-PCR or single-round real-time PCR 

analysis. Diagnostic sensitivity and specificity of the assays were determined to 

compare the performance of each method for diagnosis of Phytophthora spp. or P. 

ramorum in camellia tissues and associated potting medium. All diagnostic assays 

were highly correlated with one another and disease symptoms, with nested PCR 

having the best correlation with symptoms, followed by real-time PCR, ELISA, 

and then culture. A second research effort underway at UC Berkeley is designed to 

obtain similar data, but also investigate the influence of different hosts, environmental conditions, and other factors on the ability to accurately detect and identify 

the pathogen.

Using three regions of the nuclear genome of P. ramorum (ITS, ß-tubulin, and 

elicitin gene regions) to construct species-specific markers, Bilodeau and others 

(2006, 2007) evaluated three real-time PCR technologies (molecular beacons, 

TaqMan probes, and SYBR-Green assays) for sensitivity and specificity. The best 

performing system (TaqMan probes) was also used to compare the three DNA 

regions. Overall, TaqMan assays with ITS or elicitin had the best combination of 

sensitivity and specificity. 

Kox and others (2007) compared six methods for the detection of P. ramorum

in plants using naturally infested rhododendron plant material: isolation followed 

by morphological identification; two immunological methods, ELISA (Agdia) and 

lateral flow immunochromatgraphy (LFD, Pocket Diagnostic); and three molecular 

tests based on PCR using TaqMan chemistry, including two assays designed for 

specific detection of P. ramorum and one designed for genus-level detection of 

Phytophthora. The Phytophthora spp. TaqMan PCR, ELISA, and LFD had higher 

sensitivities than the P. ramorum-specific methods, which make them useful as 

prescreening methods, where positive results must be confirmed by PCR or isolation. The authors suggested that in critical situations (for example, in the case of a 

first finding on a new host or site), it is advisable to use both a P. ramorum TaqMan 

assay and culture. For routine testing, in most cases, it will be sufficient to rely on 

the TaqMan results.
29

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

A PCR-based mitochondrial DNA detection system for determining if a Phytophthora species was present in symptomatic plant tissue and clarifying if it was P. 

ramorum, P. nemorosa, or P. pseudosyringae was developed by Martin and others 

(2004). Results obtained with their system correlated well with the results obtained 

at the California Department of Food and Agriculture (CDFA) diagnostics laboratory 

for pathogen recovery from symptomatic tissue, and with PCR amplification for 

P. ramorum, using the rDNA ITS P. ramorum-specific primers of Garbelotto and 

others (2002b). For P. ramorum, no differences in results were obtained; all samples 

that scored positive for P. ramorum in the CDFA laboratory also were positive with 

the mitochondrial markers. The results for four of these samples were validated by 

sequence analysis of the Phytophthora genus-specific amplicon and comparison 

with data from purified cultures of this pathogen. The mitochondrial marker system 

also identified 16 additional samples infected with other Phytophthora spp. that 

could not be identified with the ITS marker system (Martin and others 2004).
30

GENERAL TECHNICAL REPORT PSW-GTR-234
31

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Chapter 3: The Disease Cycle

Background

The effective management of any plant disease is based on an understanding of 

the disease cycle, including the pathogen’s modes of survival and dissemination, 

and the role of environmental factors in disease development. The disease cycle, 

or disease process, consists of several stages, including production of inoculum, 

dispersal of inoculum, establishment of infection (entry into the host), colonization 

(invasion), symptom development (interaction of the pathogen with the host), and 

survival. Those stages—except for symptoms, which were discussed in chapter 

2—are discussed below for Phytophthora ramorum Werres, de Cock, and Man in’t 

Veld.

A diagrammatic disease cycle for P. ramorum (Courtesy N. Ochiai; reproduced 

with permission from Parke and Lucas 2008) is presented in figure 1. Although at 

first glance the P. ramorum disease cycle appears complex because of the different 

habitats and range of hosts involved, it follows the basic steps of any plant disease 

cycle. In general, Phytophthora species that infect aerial parts of plants spread 

through production of asexual sporangia and zoospores. Survival structures such 

as chlamydospores, or sometimes sexually produced oospores, may also have a 

role in dissemination and spread in those species that produce one or both of these 

structures. Disseminated spores can then initiate infections of host tissue. The new 

infections can serve as another source of spores to begin the cycle again. Appropriate environmental conditions (temperature and relative humidity), as well as a 

means of pathogen survival (either as spores or mycelia), are necessary for each 

step of the cycle. Transport of infected host tissue or contaminated growing media 

or soil containing the pathogen can introduce the disease to new areas where the 

pathogen may establish if it can complete the cycle described above (Davidson and 

Shaw 2003).

Inoculum Production 

This is the stage of the disease cycle where the pathogen produces a structure or 

structures to initiate infection. 

Types of Inoculum

Like most Phytophthora spp., P. ramorum produces asexual sporangia, zoospores, 

and chlamydospores in culture and in nature (Parke and others 2002a; Rizzo and 

others 2002a, 2005; Werres and others 2001). Sexual structures—oogonia, antheridia, and oospores—have not yet been found in nature (see for example: Ivors and 
32

GENERAL TECHNICAL REPORT PSW-GTR-234

others 2006b, Prospero and others 2007). The production of sexual oospores has 

only been observed in the laboratory. The pathogen is heterothallic and pairing 

of opposite mating types is needed for sexual reproduction. In artificial pairings, 

oospores have been observed in plants and on agar medium (Boutet and Chandelier 

2009, Brasier and Kirk 2004, Werres and Zielke 2003), but the mating system may 

not be fully functional (Boutet and Chandelier 2009, Brasier and others 2007).

Additional multihyphal reproductive structures, similar to sporodochia of 

mitosporic fungi, were produced by P. ramorum on fruits and adaxial leaf surfaces 

following inoculation (isolates or isolate source not stated) of some woody Mediterranean shrubs (strawberry tree [Arbutus unedo L.], carob bean [Ceratonia siliqua

L.], bay laurel [Laurus nobilis L.], mastic [Pistacia lentiscus L.], Italian buckthorn 

[Rhamnus alaternus L.] and Viburnum tinus L.) (Moralejo and Descals 2006, 

Moralejo and others 2006). Occasionally sporangia and chlamydosori (packed 

Figure 1—Proposed disease cycle for Phytophthora ramorum in forests. Source: Parke and Lucas 2008.
33

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

clusters of chlamydospores) were formed on the stromata after emergence through 

the adaxial leaf surface. Although these structures have not been observed in 

nature, Moralejo and others (2006) suggested that the subepidermal position of the 

stroma initials may protect the pathogen from a dry atmosphere or solar radiation, 

or that they serve as over-summering survival structures.

Host Impacts on Sporulation

Sporulation can be affected by a variety of biotic and abiotic factors, including host 

and factors of the environment such as rainfall, temperature, light, and humidity.

Host and production of sporangia and chlamydospores—

The production of sporangia and chlamydospores differs with the foliar host; some 

hosts support rapid and prolific reproduction, whereas other hosts do not (table 4). 

Davidson and others (2002b, 2005b) found abundant sporangial formation on moistened leaves of infected California bay laurel (Umbellularia californica (Hook. & 

Arn.) Nutt.) and Rhododendron spp. within 72 hours in the laboratory. Chlamydospores were also observed on the surface of moistened bay leaves. Under natural 

conditions, chlamydospores are produced within host tissues and do not appear to 

be adapted for dispersal.

Parke and others (2002a) reported that the production of sporangia, zoospores, 

and chlamydospores of P. ramorum (source of isolates not mentioned) on inoculated 

leaf disks was greatest and most rapid on California bay laurel compared to other 

hosts tested (tanoak [Lithocarpus densiflorus], madrone [Arbutus menziesii] Pacific 

rhododendron [Rhododendron macrophyllum], evergreen huckleberry [Vaccinium 

ovatum]), and at the time nonhosts (vine maple [Acer circinatum], salal [Gaultheria 

shallon], red alder [Alnus rubra], Oregon white oak [Quercus garryana]); abundant 

sporangia and active zoospores were released within 24 hours, and zoospores 

continued to be released for several days (table 4). The authors found that tanoak 

also supported production of numerous sporangia and zoospores soon after infection, usually within 24 hours. On madrone leaf disks, only chlamydospores were 

produced. Sporangial production on other species tested ranged from a few to many 

over the course of several days, with chlamydospore production following. Of the 

nonhost species tested, inoculum production was most abundant on vine maple 

and salal (Parke and others 2002a). These two species have since been reported as 

occasional hosts in nature.

Detached-leaf assay tests in the United Kingdom (U.K.) (Turner and others 

2005), using two EU1 European isolates (BBA 16/99 and 1604) and two (NA1) 

North American isolates (0-217 and 1004.1) of P. ramorum on ornamental and 

understory hosts, also found that sporulation potential differs with host species 
34

GENERAL TECHNICAL REPORT PSW-GTR-234

Table 4—Host leaves supporting sporulation of Phytophthora ramorum

Propagule type

Host Sporangia Chlamydospores Reference

California/Oregon hosts Parke and others 2002a; 

 Davidson and others 2002b,

California bay laurel (Umbellularia californica + + 2005b 

 (Hook. & Arn.) Nutt.)

Tanoak (Lithocarpus densiflorus (Hook. & Arn.) 

 Rehder) + +

Ornamental rhododendron (Rhododendron sp.) + -

Pacific rhododendron (Rhododendron + +

 macrophyllum D. Don ex G. Don)

Evergreen huckleberry (Vaccinium ovatum Pursh) + +

Vine maple (Acer circinatum Pursh) + +

Salal (Gaultheria shallon Pursh) + +

Red alder (Alnus rubra Bong.) + +

Oregon white oak (Quercus garryanna Dougl. 

 ex Hook.) + +

Madrone (Arbutus menziesii Pursh) - +

Coast redwood (Sequoia sempervirens (Lamb. ex Maloney and others 2005,

 D. Don) Endl.) + + 2007

Coast live oak (Quercus agrifolia Née) + + Vettraino and others 2008

Europe, ornamental and understory hosts DEFRA 2006, Turner

 and others 2005

Lilac (Syringa vulgaris L.) + +

Pieris (Pieris japonica (Thunb.) D. Don ex G. Don) + -

Mountain laurel (Kalmia latifolia L.) + -

Camellia (Camellia japonica L.) + -

California bay laurel (Umbellularia californica

 (Hook. & Arn.) Nutt.) + +

Ponticum rhododendron (Rhododendron ponticum L.) + +

Dog rose (Rosa canina L.) + +

Black elderberry (Sambucus nigra L.) + -

European ash (Fraxinus excelsior L.) + +

Honeysuckle (Lonicera periclymenum L.) + -

Sycamore maple (Acer pseudoplatanus L.) + -

Wych elm (Ulmus glabra Huds.) + +

Crabapple (Malus sylvestris (L.) Mill.) + -

English yew (Taxus baccata L.) + +

Bramble blackberry (Rubus fruticosus L.) + -

English ivy (Hedera helix L.) + -

European cranberrybush (Viburnum opulus L.) + +

Lingonberry (Vaccinium vitis-idaea L.)

Bearberry (Arctostaphylos uva-ursi (L.) Spreng.)
35

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

(table 4). The two NA1 isolates were generally less vigorous in sporulation than 

the two EU1 isolates. Chlamydospore production was generally less abundant than 

sporangial production (Turner and others 2005). 

In detached-leaf assays to determine sporulation on the leaves of European 

tree species (Denman and others 2006), European ash (Fraxinus excelsior) supported consistently high sporulation, whereas significantly fewer sporangia were 

observed on horse chestnut (Aesculus hippocastanum) and sessile oak (Quercus 

petraea) (table 4). In tests on English oak (Q. robur), holm oak (Q. ilex), catawba 

rhododendron (R. catawbiense) and turkey oak (Q. cerris), holm oak and catawba 

rhododendron supported more sporangia than English oak and turkey oak. Differences among the EU1 and NA1 isolates were not mentioned.

The results of detached-leaf assays using plants of Mediterranean evergreen oak 

forest and maquis-type vegetation (Moralejo and Hernández 2002) are presented in 

table 4.

European tree species Denman and others

 2006

Horse chestnut (Aesculus hippocastanum L.) +

Sweet chestnut (Castanea sativa Mill.) +

European ash (Fraxinus excelsior L.) +

Turkey oak (Quercus cerris L.) +

Holm oak (Quercus ilex L.) +

Sessile oak (Quercus petraea (Matt.) Liebl.) +

English oak (Quercus robur L.) +

Common lilac (Syringa vulgaris L.) +

English elm (Ulmus procera Salisb.) +

Catawba rhododendron (Rhododendron catawbiense Michx.) +

Woody Mediterranean species Moralejo and Hernández

 2002

Holm oak (Quercus ilex L.) + +

Italian buckthorn (Rhamnus alaternus L.) + -

Strawberry tree (Arbutus unedo L.) + +

Laurustinus viburnum (Viburnum tinus L.) + +

Mastic tree (Pistacia lentiscus L.) + +

Table 4—Host leaves supporting sporulation of Phytophthora ramorum (continued)

Propagule type

Host Sporangia Chlamydospores Reference
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GENERAL TECHNICAL REPORT PSW-GTR-234

Mycelial colonization and chlamydospore formation in xylem tissue beneath 

infected bark has been observed in some hosts (Brown and Brasier 2007, Parke 

and others 2008). Sporangial production on attached, infected bark of tree hosts 

probably does not occur, or occurs rarely and is insignificant (Davidson and others 

2005b, 2008; Garbelotto and others 2003a; Tjosvold and others 2002c). However, 

sporulation has been observed on detached bark from tanoak and coast live oak (Q. 

agrifolia) cankers floated on water (Davidson and Shaw 2003).

Epidemiologically important hosts—

Phytophthora ramorum apparently does not sporulate on bleeding bole cankers 

of bark hosts. (Davidson and others 2002b; DEFRA 2005a, 2006; Garbelotto 

and others 2003a). Sporangia occasionally observed in ooze from bleeding trunk 

cankers are considered external contaminants. In a study of infected coast live oaks 

and tanoaks in California (Tjosvold and others 2002c), less than 2 percent of the 

isolations attempted from the ooze were positive, and no spores were observed in 

the ooze. All tests for inoculum production on coast live oak cankers (incubation 

of cankers in growth chambers; pieces of cankered bark in moist chambers), were 

negative for spore production (Davidson and others 2005b), and P. ramorum was 

not found on the surfaces and exudates of cankers of infected coast live oak bark. 

Because sporulation on oak wood is apparently rare, true oak species have been 

regarded as noncontagious dead ends in the life cycle of the pathogen (Davidson 

and others 2005b, Garbelotto and Rizzo 2005). Tree hosts that are susceptible to 

trunk infections producing bleeding cankers, but not susceptible to foliar infections, 

do not provide their own inoculum, and are therefore referred to as terminal tree 

hosts. 

Several tree canker hosts are also foliar hosts. Tanoak is a canker and foliar 

host that produces inoculum on leaves. Vettraino and others (2008) have reported 

P. ramorum infecting leaves of several coast live oak saplings in the forest, and the 

potential of coast live oak foliage to produce sporangia and chlamydospores after 

inoculation in vitro (table 4). The epidemiological role of those leaf infections in the 

field is not known. 

In California mixed-evergreen forests where coast live oak and California bay 

laurel are the dominant species, infections on California bay laurel are the main 

producer of P. ramorum inoculum (sporangia) (Davidson and others 2005b, 2008). 

Sporangia are also produced on infected shoots and leaves of tanoak and coast 

redwood (Sequoia sempervirens) in coastal redwood forests (dominated by coast 

redwood, tanoak, and California bay laurel), but the sporulation rate in California 

bay laurel is significantly higher than for tanoak (Davidson and others 2008).
37

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

In California forests, sporangia produced on tanoak are a significant source 

of inoculum in some situations (Davidson and others 2005b, Maloney and others 2005). In plots with few California bay laurel stems, high disease levels were 

associated with the presence of understory tanoaks (Maloney and others 2005). 

The pathogen has been confirmed on tanoak in a Bishop pine (Pinus muricata D. 

Don)-tanoak forest at a campground within a state park just north of Fort Bragg in 

coastal northern California. California bay laurel is not found within or adjacent 

to the campground area (COMTF 2009). Pacific rhododendron is also considered a 

significant spore-producing host, but it produces lower numbers of sporangia than 

California bay laurel or tanoak shoots and leaves (Davidson and others 2002b). The 

pathogen sporulates on new infections on coast redwood needles and shoots (Maloney and others 2007) (table 4), but at significantly lower levels than on California 

bay laurel leaves and tanoak leaves and shoots (Garbelotto 2004, Garbelotto and 

Rizzo 2005). 

Studies in California have shown a clear association between the presence of 

the foliar host California bay laurel and P. ramorum infection on true oak species 

(Kelly and Meentemeyer 2002, Swiecki and Bernhardt 2001), indicating the importance of California bay laurel in the disease cycle of the pathogen in California 

forests. The presence and abundance of California bay laurel within plots was 

identified as a significant plot-level predictor of disease risk (Swiecki and Bernhardt 

2001). Several related variables, including counts and percentage canopy cover of 

California bay laurel trees within the study plot, were significant predictors of P. 

ramorum risk (Swiecki and Bernhardt 2004), showing that disease risk increases 

with increasing California bay laurel density and cover within 8 m of a coast live 

oak. Disease risk and severity were greatest at California bay laurel foliage-coast 

live oak trunk distances of 1.5 m or less, and were minimal at a distance of 10 m 

or more (Swiecki and Bernhardt 2008). Bay laurel cover within 2.5 m of the trunk 

was the best single predictor of disease risk and severity. The results suggest that 

removing California bay laurel from within 2.5 m of the trunk of a susceptible oak 

will greatly reduce, but not eliminate, the risk of disease. 

In addition to the association between the presence of California bay laurel and 

the risk of P. ramorum infection, higher abundance of California bay laurel is associated with greater levels of infection (Condeso and Meentemeyer 2007, Maloney 

and others 2005, Meentemeyer and others 2008b).

In general, coast live oak and California black oak (Quercus kelloggii Newb.) 

mortality increases with increasing amounts of inoculum on leaves of California 

bay laurel (Rank and others 2010). Although genetic variation in susceptibility to 

P. ramorum occurs in California bay laurel, local environmental factors (especially 
38

GENERAL TECHNICAL REPORT PSW-GTR-234

temperature and moisture) rather than genetics mediates expression of susceptibility 

in nature (Anacker and others 2008).

Although not a common occurrence in California forests, establishment of P. 

ramorum in tanoak forests without California bay laurel appears to be the typical 

situation in forests in southwestern Oregon (Rizzo and others 2005). Initial infection and inoculum production in Oregon tanoak stands apparently occurs on leaves 

and twigs in the upper crowns of tanoak trees. Examination of tanoak trees with 

green foliage but with bole cankers and adjacent green trees without bole cankers, 

found P. ramorum leaf and twig lesions in upper crowns of 11 of 15 tanoak trees 

with bole cankers, and from 3 of 12 nearby canker-free trees. Infected rhododendron and huckleberry in the understory were found only in the immediate vicinity 

of cankered trees (Hansen and others 2006b). 

In Europe, a parallel situation exists, with Rhododendron ponticum serving as 

the key sporulating host from which inoculum can spread to susceptible tree hosts. 

Most tree stem infections in the United Kingdom (principally on European beech 

[Fagus sylvatica L.]) and individuals of several oak species) and The Netherlands 

(European beech and American northern red oak, Quercus rubra L.) have been 

associated with direct proximity to infected R. ponticum plants in the understory 

(Brasier and Jung 2006, Brasier and others 2006a, Brown and others 2006, 

Sansford and Woodall 2007). In addition to R. ponticum, other hosts (holm oak, 

sweet chestnut, bilberry [Vaccinium myrtillus L.]) have been suggested as being 

potentially significant sources of inoculum for tree infection in northern Europe 

(Inman and others 2005, Sansford and others 2009). In southern Europe, foliar hosts 

including holm oak, Italian buckthorn, and mastic tree produce significant inoculum (Moralejo and others 2007) and may contribute to increased disease levels in 

Mediterranean forests and in maquis shrubland (Sansford and others 2009).

Environmental Factors Affecting Sporulation and Germination

Laboratory studies—

Phytophthora ramorum produces spores under a broad range of temperature and 

light conditions. In a laboratory study of four U.S. isolates (NA1) and three European isolates (EU1) of P. ramorum, chlamydospores were produced by U.S. isolates 

at 10 to 28 °C (optimum of 14 to 24 °C, depending on isolate), and by EU isolates at 

10 to 26 °C (optimum of 22 to 26 °C), with one isolate producing chlamydospores 

at 6 °C (Englander and others 2006). Sporangia were produced at all temperatures 

tested: 10 to 30 °C (optimum of 16 to 22 °C, depending on isolate) for U.S. isolates, 

and 6 to 26 °C (optimum of 22 °C) for EU isolates. The U.S. isolates grew less and 

produced fewer sporangia and chlamydospores when exposed to increasing doses of 
39

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

near-UV radiation and visible radiation. The EU isolates were exposed to near-UV 

only, which significantly reduced growth of one of three isolates, but had no significant effect on spore production (Englander and others 2006). 

Differences in humidity had the greatest effect on sporangial production and 

zoospore germination in vitro, whereas sporangial germination was less sensitive 

(Turner and Jennings 2006, 2008). Maximum levels of sporangial production and 

zoospore germination occurred at 100 percent humidity.

In laboratory trials, zoospore production on California bay laurel leaves was 

influenced by temperature (Davidson and others 2005b). Zoospores were produced 

at 5, 10, 15, 20, and 25 °C, but not at 30 °C, with the highest numbers released at 

15 to 20 °C. Turner and Jennings (2006) reported that optimum temperature for 

sporulation and zoospore germination ranged from 20 to 30 °C depending upon 

experimental conditions.

On agar media (V8, cornmeal with antibiotics [CAR], and water agar plates), 

chlamydospore germination rate (0.5 to 10.7 percent) (isolate source not stated) after 

24 hours was low and variable compared with published chlamydospore germination rates of other Phytophthora species (Smith and Hansen 2008). 

Forests/woodlands—

In California mixed-evergreen forests, sporulation and production of inoculum are 

seasonal, largely dependent on rainfall events and temperature. In California, P. 

ramorum is commonly recovered from rain traps from December into the spring 

months, peaking during warm rains in May (Davidson and others 2005b). At one 

study site in a mixed-evergreen forest, sporulation of P. ramorum was correlated 

with rain events and air temperature (Davidson and others 2005b). Detectable levels 

of P. ramorum inoculum were present largely during the period of winter rains, and 

were absent during the hot, dry summer (Davidson and others 2005b). The authors 

observed a lag period between the start of the rains and the onset of detectable 

inoculum production at the site, with the highest levels of spore production occurring at the end of the rainy season. Possible explanations include the need for some 

time for inoculum to build up as California bay laurel leaves become infected, or 

the occurrence of lower air temperatures during the beginning of the rainy season, 

which would inhibit sporangial production (Davidson and others 2005b, Fichtner 

and others 2006). 

Recovery of P. ramorum from rain traps at five plots in a redwood/tanoak forest 

type did not show a lag period, with sporangial production beginning soon after the 

start of the rainy season (Maloney and others 2002, Rizzo and others 2005). Explanations for the sporangial production in redwood/tanoak woodlands being earlier 

than in mixed-evergreen forests include less shedding of California bay laurel 
40

GENERAL TECHNICAL REPORT PSW-GTR-234

leaves and more active lesions on California bay laurel leaves after the hot summer 

period because of the wetter, cooler conditions in the redwood/tanoak forest type 

(Davidson and others 2005a).

In contrast, P. ramorum inoculum (most likely dehiscent sporangia) in infested 

forests of southwest Oregon can be produced throughout the year whenever there is 

water available (Hansen and others 2008). The authors found inoculum on infected 

tanoak leaves and twigs during periods of leaf wetness, even in extended periods 

without rain but only fog, any time during the year. 

Spore production varies yearly as well as seasonally. In California forests, 

relatively high levels of winter/spring rainfall extending into early summer are often 

followed by high levels of disease (Davidson and others 2005b, Rizzo and others 

2005). Epidemic mortality of coast live oak occurred 1 to 2 years after increased 

spring rainfall in 1998 and again in 2005 (El Niño years) (Davidson and others 

2005b, Rizzo and others 2005). In Oregon, Kanaskie and others (2008a) attributed 

an unexpected and large amount of disease expansion from eradication sites to 

two consecutive years of unusually wet spring and early summer weather. Hansen 

and others (2008) reported that late May rains following a dry April triggered an 

infection event at two sites, resulting in dieback and new growth of tanoak and 

rhododendron, and numerous new P. ramorum bole infections. These data point to 

the importance of changes in climate in the establishment and spread of a largely 

aerial pathogen such as P. ramorum (Rizzo and others 2005). 

Inoculum Dispersal 

Phytophthora ramorum inoculum produced on host tissue may be spread or dispersed by various means. Local dispersal is by rain splash or wind-driven rain, 

intermediate dispersal is thought to occur by turbulent air, and long-distance 

dispersal occurs primarily through the movement of infected plant material moved 

in trade; movement of contaminated soil or spread in watercourses can also result in 

long-distance dispersal. Other undetermined mechanisms are also likely.

Local Dispersal

Local dispersal occurs primarily through rain splash of sporangia (Davidson and 

others 2002b). Rain splash from leaves and soil is the primary means by which 

inoculum is dispersed from infected leaves in the shrub canopy to tree stems or 

from leaves in the overstory to hosts below. Infested soil may serve as primary 

inoculum for foliar infection of California bay laurel and tanoak by splash dispersal 

during rain events (Fichtner and others 2009a). Infection of conifer seedlings and 

rhododendron placed under infected California bay laurel occurred only during 
41

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

periods of precipitation and only when the plants were within 4.4 m of the infested 

overstory (Chastagner and others 2008d).

Wind Dispersal

In California, inoculum has been shown to be dispersed up to 15 m during winddriven events (Davidson and others 2005b). High winds associated with storm 

events may blow raindrops with spores even farther, thus serving as a means of 

longer distance dispersal (Davidson and others 2005b). In the United Kingdom, P. 

ramorum has been detected in spore traps at least 50 m from the nearest source of 

inoculum (Turner 2007b, Turner and others 2008a).

In southwest Oregon, most new infections occur within 300 m of infected 

trees, but rare events lead to dispersal up to 4 km (Hansen 2008a). Hansen (2008a, 

2008b) has suggested that the observed dispersal over hundreds of meters in Oregon 

forests could be explained by turbulent dry air dispersal. Hansen hypothesized that 

clearing weather following spring rains results in overnight dew and fog, with the 

lifting of fog as day progresses resulting in lofting of sporangia; the sporangia are 

carried by prevailing winds and settle on fog-moistened host leaves in the evening 

to initiate infection. 

Long-Distance Dispersal

Movement of host material—

Movement of infected plant material (for example, wood, green material products, 

and especially nursery stock) is a primary means of long-distance spread of many 

pathogens, including P. ramorum. International trade in ornamental plants is 

postulated as a main driver for the initial emergence of P. ramorum (Davidson and 

Shaw 2003). Local, national, and international trade in plants and plant products 

is a major pathway by which P. ramorum arrives in new areas and spreads once 

it reaches them. It is the main pathway for long-distance spread of the pathogen, 

which is carried on foliage and stems and also in the associated growing medium 

(see for example, Prospero and others 2009). In the United States, the dispersal of 

the pathogen nationwide from one nursery has been documented (Frankel 2008, 

Garbelotto and Rizzo 2005, Stokstad 2004), and is discussed in chapter 2. All three 

identified lineages of this pathogen have been detected in some U.S. nurseries (Ivors 

and others 2006b), indicating that the commercial nursery trade is unknowingly 

aiding the movement, and probably the introduction, of P. ramorum into North 

America (Garbelotto 2004, Goss and others 2009b, Mascheretti and others 2008, 

Prospero and others 2009). In Europe, P. ramorum was introduced to Majorca, 

Spain, via a shipment of infected rhododendrons, and many of the infections found 
42

GENERAL TECHNICAL REPORT PSW-GTR-234

in nurseries in the United Kingdom can be traced to plant transport from other 

nurseries (Davidson and Shaw 2003). Phytophthora ramorum has continued to be 

found on material having a plant passport (see chapter 5) in England and Wales 

(Slawson and others 2008), supporting the view that the pathogen is continuing to 

move in trade. 

Watercourses—

Propagules of P. ramorum are dispersed readily in stream water. Contaminated 

watercourses represent a potential pathway for pathogen spread, especially if water 

is used for the irrigation of susceptible plants. Davidson and others (2005b) detected 

inoculum by baiting stream water 4 to 6 km from an inoculum source in a coast 

live oak-bay laurel forest. The pathogen is regularly recovered from streams draining infested sites in Oregon, even 5 years after eradication treatment (Goheen and 

others 2008). The U.S. Department of Agriculture, Forest Service (USDA FS) has 

developed a national P. ramorum stream monitoring program for the early detection 

of P. ramorum infestation in the United States (Oak and others 2006, 2008). As a 

result of these activities, 12 first detections of P. ramorum have been made in seven 

states from 2006 through 2008 (Oak and others 2010). In the United Kingdom, 

P. ramorum can be found in watercourses at outbreak sites (Turner 2007b). At an 

infested site in West Sussex, P. ramorum was recovered from the river catchment 

area originating from the site, but inoculum disappeared within a few kilometers 

downstream of the outbreak source (Turner 2007b). 

Monitoring of inoculum levels in water has shown seasonal patterns in amounts 

of inoculum in California and the United Kingdom. In California, the pathogen has 

been detected in water samples taken from streams during the winter/spring rainy 

season, but only at reduced levels in the summer months (Davidson and others 

2005b). Tjosvold and others (2002b) recovered P. ramorum very rarely (on one 

occasion in September from one river following a short rain in the river's drainage) 

during the dry summer months. In a study using rhododendron leaf baits placed 

in California streams within a redwood/tanoak forest (Maloney and others 2002), 

detection was reported in both spring and summer months, regardless of any rain 

event. At U.K. study sites, the highest levels of inoculum, as detected by rhododendron leaf baits, generally occurred in winter and spring and the lowest levels in 

summer (DEFRA 2007, Turner 2007b, Turner and others 2008a). In another U.K. 

study, baiting of watercourses within a garden infested with P. ramorum generally 

showed low levels of P. ramorum in the summer and winter, but samples taken 

in the spring, and to a lesser extent in the autumn, were frequently positive for P. 

ramorum (Lockley and others 2008). In contrast, no seasonal effect on recovery 

from streams has been found in Oregon (Sutton and others 2009).
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Soil—

Human movement of soil infested with P. ramorum is a means of local as well as 

longer distance dispersal. Although there is no direct evidence of new P. ramorum

infections occurring in forest situations as a result of human movement of infested 

soil, soil attached to hikers’ boots and vehicles has been shown to contain the 

pathogen. In studies conducted in Sonoma County California, symptom levels and 

spread of the pathogen were greater in areas with high human activity (Cooper and 

Cushman 2006; Cushman and Meentemeyer 2006a, 2006b). In the spring rainy 

periods, baiting for P. ramorum yielded a 40 to 60 percent recovery rate for trail 

soil and 40 to 95 percent recovery rate for soil removed from hikers’ shoes; the 

pathogen was not recovered from trail soil or shoe soil in the dry summer period 

(Tjosvold and others 2002a). Davidson and others (2005b) also demonstrated human 

spread of infested soil during the rainy season. When they baited soil taken from 

hikers’ shoes after they walked a preserve trail in Sonoma County California, the 

pathogen was recovered from 7 of 15 samples in one trial and from 5 of 15 samples 

in a second trial. Hikers dispersed P. ramorum in soil on their shoes a distance of 

at least 60 to 100 m into areas of a nature reserve in California that lacked local 

inoculum sources (Cushman and others 2008). If the soil was kept moist, P. ramorum could be isolated from the soil up to 72 hours after the infested soil was picked 

up by hikers (Cushman and others 2008). 

In U.K. studies, Phytophthora spp. were present in about 30 percent of samples 

collected from boots prior to disinfection upon leaving woodland outbreak sites. 

The most commonly occurring species was P. citricola, but 10 to 15 percent of the 

samples contained P. ramorum or P. kernoviae (Webber and Rose 2008). 

Other agents—

Although it has been suggested that insects may vector spores or sporangia of the 

pathogen (McPherson and others 2002b), no evidence of insect transmission has 

been found (DEFRA 2005a, Kanaskie and others 2002, McPherson and others 

2002b). Birds have also been suggested as vectors, but as with insects, no evidence 

of birds serving as vectors of P. ramorum has been demonstrated. In laboratory 

studies (Parke and others 2008), feces from gray garden slugs (Deroceras reticulatum) that were fed cultures of P. ramorum or allowed to graze on infested leaves 

contained viable chlamydospores, sporangia, and hyphae of the pathogen. Under 

controlled conditions, P. ramorum was transmitted by slugs or their feces to rhododendron leaves and to tanoak leaves and logs (Parke and others 2008).

Dispersal in nurseries—

Local dispersal of P. ramorum in nurseries and garden centers occurs by many 

of the same means as in the forest. The pathogen may be transmitted through 
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GENERAL TECHNICAL REPORT PSW-GTR-234

plant-to-plant contact, rain or overhead irrigation splash dispersal, irrigation and 

the movement of infested debris, growing media, and freestanding water or surface 

water runoff. In experiments designed to compare relatively long-distance (1 to 4 

m) and short-distance (pot-to-pot) dispersal among rhododendrons in simulated nursery conditions, new infections were only detected on plants within a short distance 

(adjacent and up to 30 cm away) of a centrally located artificially infected plant 

(Tjosvold and others 2006b). No infection was detected in the long-distance experiments and no inoculum was detected in rain traps located 1 to 4 m away from the 

infected plant during rain events. Note, however, that sporangia have been detected 

up to 5 m from infested forest canopy (Davidson and others 2002b), demonstrating 

that height of release influences distance of splash. Werres and others (2007) demonstrated survival of P. ramorum in nursery water reservoirs containing contaminated irrigation water during all seasons. Disease symptoms on rhododendron were 

observed in as little as 7 days after irrigation with contaminated water.

Infection

In the infection stage of the disease cycle, the pathogen germinates, penetrates the 

host, and establishes a parasitic relationship with the host plant.

Environment

Phytophthora ramorum is considered a cool-temperature organism, with optimal 

growth between 18 and 22 °C (Werres and others 2001). Germination of P. ramorum sporangia may be direct, by emergence of hyphae through the sporangial 

wall, or indirect, by formation and release of motile zoospores. With many species 

of Phytophthora, indirect germination predominates at temperatures below about 

12 oC, and direct germination occurs at higher temperatures (Ribeiro 1983). The 

presence of free water or high humidity favors zoospore germination and infection. 

Maximum levels of zoospore germination occurred at 100 percent humidity or 

water potentials of 1; a broad range of temperatures (10 to 30 °C depending on the 

water potential) supported zoospore germination (Kessel and others 2007, Turner 

and Jennings 2008). The infection rate for California bay laurel leaves averaged 92 

percent at 18 °C, but only 50 percent at 12 °C and 37 percent at 30 °C (Garbelotto 

and others 2003a). 

Free water enhances infection. A minimum of 6 to 12 consecutive hours of free 

water is a prerequisite for the infection of California bay laurel leaves (Garbelotto 

and others 2003a). Infection by zoospores tends to occur on susceptible plant parts 

where water accumulates, such as at leaf tips. 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Infection Courts

Openings in host tissue—either natural openings such as stomata or lenticels, 

or wounds—are entry courts for hyphae originating from germinated spores 

(Florance 2002, 2006; Inman and others 2005). The likely sites of initial infection 

on Camellia leaves were stomata on adaxial surfaces, as well as subepidermal oil 

glands (Geltz and others 2006). 

Studies by Lewis and Parke (2006) suggested that wounded tissue of Rhododendron leaves was more susceptible to infection than nonwounded. Using 

scanning electron microscopy, they observed that germinating cysts were more 

abundant at wound sites than at stomatal openings. A study in the United Kingdom 

(DEFRA 2005a) found that infection occurred when lower leaf surfaces, where 

stomata occur, were inoculated, but did not occur when unwounded upper leaf 

surfaces with no stomata were inoculated. A separate experiment (DEFRA 2005a) 

found that some hosts (Camellia japonica) required leaf wounding for infection to 

occur, whereas others (R. ponticum, R. catawbiense, Fraxinus excelsior) did not. 

Hansen and others (2005) reported many species developed substantial leaf necrosis 

in leaf dip inoculation, but few or no leaf symptoms from plant dip inoculation, the 

difference possibly being—in addition to a higher effective inoculum dose as well 

as more favorable incubation conditions—the wounds provided on detached leaves.

Phytophthora ramorum zoospores are capable of directly penetrating bark of 

mature trees. Brown and others (2006) reported that P. ramorum zoospores were 

able to penetrate intact European beech bark. Wounding of mature European beech 

(Fagus sylvatica L.) logs, American red oak (Quercus rubra L.), sweet chestnut, 

English oak, Sitka spruce (Picea sitchensis (Bong.) Carrière) and Douglas-fir 

(Pseudotsuga menziesii (Mirb.) Franco) was not necessary for the infection of logs 

from mature trees by zoospores (Webber 2004). Inoculations resulted in infection 

and phloem necrosis development 2 weeks after inoculation of intact bark in the 

absence of any wound. Infection occurred most frequently in the thin-barked species (American red oak, sweet chestnut, European beech). 

Bark of saplings of some tree hosts is less susceptible to direct bark infection 

than bark of mature trees (DEFRA 2005a). Three-year-old saplings of various 

species (Douglas-fir, sweet chestnut, American red oak, English oak, Sitka spruce, 

wild cherry (Prunus avium (L.) L.), European beech, horse chestnut, small-leaved 

linden (Tilia cordata Mill.), European ash, sycamore maple, and hornbeam (Carpinus betulus L.) were only infected when wounded, and trees were more susceptible 

in the summer than in the winter, with Sitka spruce, horse chestnut, and hornbeam 

not developing symptoms following winter inoculations (DEFRA 2005a).
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GENERAL TECHNICAL REPORT PSW-GTR-234

Swiecki and Bernhardt (2006) reported that bark thickness and unweathered 

brown tissue within bark fissures of coast live oak were positively correlated with 

P. ramorum disease risk. The authors suggested that those areas of bark expansion 

tissue may represent relatively rapidly expanding regions of the outer bark in fastgrowing trees that may be more easily breached by P. ramorum zoospores. Alternative suggestions include that the outer periderm in these areas may be so thin that 

plant substances can diffuse from them when the bark surface is wet, which may 

attract P. ramorum zoospores, increasing the chance of infection, or that the bark 

fissures may be wetter longer than other areas of the bark, which would also favor 

infection.

Although P. ramorum has not been reported to cause root infection on mature 

trees, several reports of root infection by the pathogen occur in the literature. Root 

infection of tanoak seedlings in the forest has been reported (Parke and others 

2006c). Lewis and others (2004) and Parke and Lewis (2007) reported root infection 

of 3-year-old rhododendron following replanting of the cuttings into potting soil 

containing inoculum of P. ramorum, indicating transmission of P. ramorum from 

infested potting media to stems via infected, symptomless root tissue. Isolation of 

P. ramorum from healthy-appearing rhododendron roots 4 weeks after inoculation 

of soils with chlamydospores was reported by Colburn and others (2005). Bienapfl 

and others (2005) isolated P. ramorum (NA2 lineage) from asymptomatic roots of 

commercially grown rhododendron obtained from a California commercial nursery. 

The pathogen has been isolated from asymptomatic roots in laboratory-inoculated 

host plants (Shishkoff 2007). Artificial inoculation of Viburnum tinus led to the 

formation of chlamydospores in root tissue (Shishkoff 2008), and P. ramorum has 

been reported (Fichtner and others 2008a, 2009b) from roots of naturally infected 

R. ponticum shrubs in U.K. woodlands.

Host Etiology

Host leaf age—

Host leaf age affects susceptibility (De Dobbelaere and others 2008, Hansen and 

others 2005). In detached-leaf dip assays, young leaves of tanoak and California 

bay laurel (known as myrtlewood in Oregon) were more susceptible than mature 

leaves (Hansen and others 2005). In a test of 80 different Rhododendron species 

and cultivars, De Dobbelaere and others (2008) found that leaf age affected susceptibility to P. ramorum. When using wounded leaves, young leaves of all cultivars 

tested showed a higher level of susceptibility than mature leaves. However, when 

nonwounded leaves were used, young leaves of some cultivars were less susceptible than older leaves. This effect was correlated with the presence of hairs on the 
47

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

young leaves of those cultivars, which probably form a barrier to the zoospores and 

prevent tissue penetration. 

Temperature exposure—

Exposing Rhododendron plants to high temperatures for several hours before collection of the leaves decreased susceptibility in most experiments (De Dobbelaere 

and others 2008). The authors suggest that the increase in temperature may have 

resulted in stomatal closure, which may have reduced penetration capacity.

Seasonal Variation of Log Susceptibility

Hansen and others (2005) reported smaller lesions following P. ramorum inoculation on tanoak logs harvested in January than on tanoak logs harvested in March, 

September, or November, whereas lesions on Douglas-fir inoculated in January 

were larger than at other times of the year. Brasier and Kirk (2001) observed similar 

seasonal variation in susceptibility of various trees to log inoculations with other 

Phytophthora spp. They concluded that trees in the United Kingdom were most 

susceptible in late summer and fall, and essentially immune in April.

Inoculum Pressure

The amount of inoculum (inoculum pressure) affects infection potential. Differences in susceptibility with different levels of P. ramorum inoculum have been 

reported (DEFRA 2005a, Hansen and others 2005). For example, at low inoculum 

levels (1.3 x 103 zoospores/ml), common elderberry (Sambucus nigra), lilac 

(Syringa vulgaris), California bay laurel and honeysuckle (Lonicera periclymenum

L.) were not infected in detached leaf assays with unwounded leaves. However, 

when the amount of inoculum level was increased (2.3 x 105 zoospores/ml), 67 to 

100 percent of the leaves inoculated became infected (DEFRA 2005a). The same 

study (DEFRA 2005a) found that unwounded leaves of C. japonica remained 

uninfected at both low and high inoculum pressures, but 33 percent of wounded 

leaves were infected at the low inoculum pressure and 100 percent at the high 

inoculum pressure. Hansen and others (2005) reported that inoculum dose affected 

susceptibility in detached-leaf assays, with higher zoospore concentrations generally resulting in more symptoms.

Colonization (Invasion)

The invasion stage of the disease cycle occurs when the pathogen grows on or in the 

host and obtains nutrients from it.

Following entry through the bark of woody hosts, hyphae of P. ramorum grow 

within the phloem and cambial tissues, and then into xylem tissues (Brown and 
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GENERAL TECHNICAL REPORT PSW-GTR-234

Brasier 2007, Parke and others 2007, Rizzo and others 2002a). Xylem colonization 

is the norm. Rizzo and others (2002) noted that infection on Quercus spp. and 

tanoak appeared to begin in the outer bark, progress to the cambium, and eventually reach the xylem. Discoloration was generally more extensive in the cambium 

and secondary phloem tissues than in the xylem; typically black discoloration 

extended less than 1 mm into xylem tissues, but was occasionally observed up to 

3 cm into the xylem. Brown and Brasier (2007) found that P. ramorum commonly 

occupies xylem beneath phloem lesions, that the pathogen can penetrate xylem 

tissue, and that it spreads in xylem tissue ahead of phloem lesions. Parke and 

others (2007) demonstrated that the pathogen colonized tanoak sapwood, and then 

spread through xylem vessels. Hyphae were abundant in the xylem vessels, ray 

parenchyma, and fiber tracheids; chlamydospores were observed in the vessels. The 

authors found reduced sap flux and specific conductivity in infected tissues compared to noninfected, and suggested that the reduction may result from increased 

embolism caused by P. ramorum infection, the presence of fungal structures, and 

the increased abundance of tyloses present in the vessels. They further suggested 

that the reduced stem water transport may contribute to crown mortality associated 

with P. ramorum infection. Further studies (Collins and others 2009) found that 

infection by P. ramorum induces tyloses in the xylem vessels of tanoak stems and 

demonstrated that tylosis formation is associated with reduced hydraulic conductivity of the sapwood.

Several studies have examined P. ramorum colonization of Rhododendron. 

Pogoda and Werres (2004) found that P. ramorum colonized the cortex, phloem, 

xylem, and pith of the necrotic zone. The authors also found hyphae in the cortex 

and pith of healthy-looking material about 1 cm below visible discoloration; chlamydospores were only observed in the necrotic zone where they developed mainly 

in the cortical parenchyma. This study also showed that P. ramorum can grow both 

intra- and intercellularly, but chlamydospores were only observed in the intercellular spaces. 

Using epifluorescence microscopy, Riedel and others (2008) found P. ramorum

hyphae in the cortex and pith of infected Rhododendron plants when discoloration 

was present. In healthy-looking stem and root segments located adjacent to the 

discolored areas, hyphae were found most often in the secondary xylem. With 

one exception, chlamydospores were only located in discolored parts of infected 

Rhododendron plants, being present in the cortex (stem) and palisade mesophyll 

(leaf). Less frequently, chlamydospores were observed in the pith of necrotic stem 

segments. Using the same epifluorescence microscopy technique, Parke and Lewis 
49

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

(2007) observed attraction of zoospores to wounds and root primordia of Rhododendron tissue culture plantlets in vitro, and colonization of the cortex and vascular 

tissues of roots and stems, including the xylem.

Survival

The disease potential for a pathogen, including P. ramorum, is partially dependent 

on its ability to survive during conditions unfavorable for growth and reproduction. 

Like most species of Phytophthora, P. ramorum survives during conditions unfavorable for growth—such as hot, dry summer months in California—in host tissues 

or in various nonhost substrates (such as organic matter, soil, and potting media) as 

hyphae or as asexual structures. For most species of Phytophthora, chlamydospores 

are the typical survival structures in the disease cycle. 

Survival in Vitro

In moist conditions, zoospores and chlamydospores of P. ramorum remain viable 

for at least 1 month, with chlamydospores probably able to survive much longer 

(Davidson and others 2002b). Zoospores and chlamydospores did not germinate on 

a selective medium after 30 minutes on dry filter paper. After 30 minutes on moist 

filter paper, 41 percent of chlamydospores and 20 percent of zoospores germinated. 

In deionized water, 75 percent of chlamydospores and 20 percent of zoospores 

germinated on a selective medium after 30 days (Davidson and others 2002b). 

Laboratory studies (Fichtner and others 2007) demonstrated a decline in P. ramorum survival in soil with gradual drying. 

A U.K. laboratory study (DEFRA 2005a) found that sporangia and chlamydospores germinated on agar after exposure to -2 °C for 24 hours. Chlamydospores 

were not capable of germinating after exposure to 55 °C for 1 hour. No chlamydospores germinated following exposure to 40 °C for 24 hours or -25 °C for just 4 

hours. Sporangia did not germinate after a 2-hour exposure to these temperatures. 

Sporangia germinated after 6 hours, but not 24 hours, at room temperature in dry 

conditions. In a study to determine the effects of temperature and composting 

treatments on the viability of P. ramorum (Swain and others 2006), the pathogen 

was not recovered from compost by plating on selective medium or by baiting 

with pears following temperatures of 55 °C for 1 hour or 40 °C for 24 hours. The 

pathogen was also not detected using PCR, suggesting that P. ramorum was absent 

from the treated compost and not just suppressed or dormant. Similar results 

were reported by Turner and Jennings (2006); chlamydospores germinated after 2 

months storage in vitro at 0, 5, 15 and 30 °C, but not at -25 °C or 40 °C. 
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GENERAL TECHNICAL REPORT PSW-GTR-234

Survival in Host Material

An important means of P. ramorum survival over the hot, dry summer months in 

California is in infected California bay laurel leaves (Davidson and others 2005b, 

Rizzo 2006). Survival in attached leaves was found to be higher than in abscised 

leaves (Davidson and others 2002a, 2003a). Survival (as assessed by cultural isolation) in attached bay laurel leaves declined from approximately 90 percent in June 

to 50 percent in August, but persisted throughout the summer. Survival in abscised 

leaves collected from leaf litter in June, July, and August was nearly zero. The same 

study determined that infected bay leaves were significantly more likely to abscise 

in drier mixed-evergreen forest as opposed to tanoak-redwood forest. The authors 

surmised that, given that survival of P. ramorum occurs in attached rather than 

abscised leaves, the observed differences in abscission rates of P. ramorum-infected 

bay leaves in coast live oak versus tanoak-redwood forests may be one factor 

contributing to differences in the onset of detectable inoculum production in these 

two forest types during the winter rainy season.

Fichtner and others (2008b) compared summer survival of P. ramorum associated with California bay laurel leaves in redwood-tanoak and mixed-evergreen 

forests. Pathogen isolation from attached leaves ranged from 40 to 100 percent at 

each site in May and declined to a range of 0 to 40 percent in August, with higher 

isolation recovery observed in redwood-tanoak forests than in mixed-evergreen 

forests. 

In leaf-debris survival experiments in Oregon (McLaughlin and others 2006), 

Rhododendron and tanoak leaves inoculated with P. ramorum were placed in the 

field; the leaves were shaded or unshaded, and placed above ground or buried. 

Pathogen survival was higher (89 percent) in buried leaves after 8 weeks than 

in those on the soil surface in shade (66 percent recovery) or on the soil surface 

exposed to the sun (26 percent recovery). 

Shishkoff and Tooley (2004) reported survival of P. ramorum in infected 

Rhododendron leaf tissue containing chlamydospores buried in mesh bags in potted 

nursery stock for up to 155 days after burial. In additional experiments, Shishkoff 

(2007) recovered P. ramorum from moist potting mix or sand for many months, 

whether buried as infected plant leaf tissue or as mycelia bearing chlamydospores. 

The author found no significant difference in recovery over time among treatments 

(sand or potting mix; infected plant tissue or mycelia); after approximately a year, 

colonies could be recovered at 0.8 to 14.3 percent. 

The pathogen can survive in artificially infected leaf debris buried in soil for at 

least two U.K. winters (Turner and others 2005). Chlamydospores of P. ramorum

in lilac (S. vulgaris) and rhododendron leaves, either as surface leaf litter or buried 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

5 cm deep in soil, survived the winter season in experiments conducted in northern England and Scotland (Turner and others 2005). Pathogen survival gradually 

decreased over time, but P. ramorum was recovered from at least 50 percent of 

leaves in all treatments. Survival was slightly higher on the host (rhododendron) 

that had thicker and more durable leaves compared to the host (lilac) that had more 

fragile and less durable leaves. Survival was highest on rhododendron leaves that 

had been buried 5 cm below the soil surface, with over 80 percent of leaves still 

yielding the pathogen after 4 months. Tests carried out in Scotland in a parallel 

experiment showed similar survival under ambient conditions over the same period. 

In an experiment in the Netherlands to monitor the persistence of P. ramorum after 

infected rhododendrons were cut down and chipped, the pathogen was detected up 

to 2 years later in the chips left in situ (Steeghs 2008).

The pathogen has been recovered from host tissues at eradication sites. At 

Oregon eradication sites, P. ramorum was recovered from tanoak sprouts around 

88 percent of the tanoak stumps sampled (Hansen and Sutton 2006). Initial sprouts 

were destroyed, and subsequent exams found no infection on later establishing 

sprouts or seedlings (Hansen 2007). At one eradication site in the United Kingdom, 

the pathogen was observed on new shoots emerging from cut rhododendron stumps 

(DEFRA 2007).

Phytophthora ramorum also survives, probably as chlamydospores, in wood. 

Shelly and others (2006) isolated P. ramorum from 1 of 30 specimens of tanoak and 

coast live oak logs that had air-dried for 6 months, demonstrating that P. ramorum

could survive on log for at least 6 months. Brown and Brasier (2007) reported 

survival of the pathogen in exposed wood of trees for up to 2 years.

Survival in Soil and Potting Media

In California, P. ramorum is rarely isolated from mixed-evergreen forest soils during the hot, dry summer period (Davidson and others 2002b and 2005b), although 

the pathogen survives in infected leaves in the soil or litter over the summer period, 

especially in redwood-tanoak forests (Fichtner and others 2006, 2007). Davidson 

and others (2002b, 2005b) did not recover P. ramorum from soil and litter surrounding infected oaks within a coast live oak woodland in the summer months. 

The failure to detect the pathogen in soil during the summer coincided with a drop 

in mean soil water content to less than 15 percent, indicating that seasonal drying 

is sufficient to reduce viability of spores in these substrates. Maloney and others 

(2002) also found that recovery of P. ramorum from soils dropped to zero during 

the summer months, with frequency of recovery from soil during the rainy season 

approximately 20 percent, but summer soil collections showing no P. ramorum

recovery.
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GENERAL TECHNICAL REPORT PSW-GTR-234

In contrast, Fichtner and others (2006, 2007) demonstrated that P. ramorum

survives and produces chlamydospores in forest soils over summer, providing a 

possible inoculum reservoir at the onset of the fall disease cycle. Although Davidson and others (2002a, 2005b) could not detect P. ramorum in soils associated with 

oaks within approximately 1 month of the last spring rain event, Fichtner and others 

(2006, 2007) recovered the pathogen from soils up to 3 months after the last rain 

event. Fichtner and others (2007) reported that recovery frequency of P. ramorum

was highest under California bay laurel and intermediate under tanoak, with only 

occasional recovery under redwood. Fichtner and others (2009a) reported suppression of chlamydospore production in moist, redwood-associated soils. Recovery of 

the pathogen from infected rhododendron leaf discs after 8 weeks was highest in 

the soil (80 percent), intermediate in the litter/soil interface (60 percent) and poor 

(1 percent) on the leaf litter surface. The differences between the two studies may 

be explained by the fact that Davidson and others (2002a, 2005b) monitored soil 

inoculum in a mixed-evergreen forest using pear baits, whereas Fichtner and others 

(2006, 2007) monitored soils in a redwood/tanoak forest using rhododendron leaf 

baits. 

Lockley and others (2008) reported variable results with survival of P. 

ramorum at a site in the United Kingdom. At one site, where the infected host 

(Rhododendron) was removed and composted mulch applied to the soil surface, the 

pathogen could not be detected in soil samples. At a second site, where host removal 

was impractical and the only treatment was removal of lower branches of the 

rhododendrons, detection of P. ramorum in soil samples gradually declined. In The 

Netherlands, Aveskamp and others (2006) found that the pathogen remained viable 

for at least 1 year in sandy soil. The authors reported that the pathogen was more 

abundant at a depth of 20 cm than at the soil surface.

Phytophthora ramorum has also been found at depths of up to 15 cm in soil in 

areas of severe plant infection (Turner and others 2008a). Monitoring at sites where 

eradication attempts were made early in the disease epidemic has shown that, in the 

absence of inoculum sources, residual contamination in soil declined slowly over 

time and in some cases declined to below thresholds of detection (Turner 2007a). 

At five eradication sites in Oregon, P. ramorum was recovered over a 4-year period 

from soil at the base of selected stumps at three sites, only in the initial sample at 

one site, and never recovered from soil at one site (Goheen and others 2008).

Phytophthora ramorum has a high potential for infesting and remaining 

viable in potting media. Linderman and Davis (2006b, 2006c) reported survival 

of P. ramorum in potting media or soil for up to 6 months when the pathogen was 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

introduced to the media as sporangia, and 12 months when introduced as chlamydospores. Potted Rhododendron became infected following inoculation of potting mix 

with P. ramorum (Grünwald and others 2008c). Colburn and others (2005) found 

no decline in chlamydospore populations after 4 months in sand, potting soil mix, 

or forest soil held at 4 °C, but the population declined in forest soil at 22 °C. Jeffers 

(2005) reported recovery of P. ramorum from a composite sample container mix 

(containing plants shipped from California to South Carolina retail nurseries) after 

storage for 6, 8, and 12 weeks at 4 °C, but not from another sample stored for 10 

weeks at room temperature.

In a study designed to help define treatments capable of inactivating chlamydospores in soil substrates, Tooley and others (2008) investigated germination 

potential over a 7-day temperature treatment by incubating chlamydospores in sand 

at low (0, -10, -20 oC) and high (30, 35, 40 oC) temperature treatments. Near 100 

percent germination was observed at temperatures of 0 °C for up to 7 days in the 

low temperature treatments, but almost no germination occurred at -10 or -20 °C 

over the 7-day period. For the high-temperature treatments, high levels of chlamydospore germination were observed over the 7-day period at 30 °C, whereas no 

growth was observed at 40 °C. At 35 °C, high levels of chlamydospore germination 

were observed at day 1, but recovery (growth on selective agar medium) declined 

steadily and was zero by 7 days. 

The role of P. ramorum oospores as survival structures is unknown, as they 

have not been observed in the field. In other species of Phytophthora, the thickwalled oospores typically serve as survival structures.

Summary

For any pathogen to successfully complete its disease cycle, a suitable environment 

and the presence of a susceptible host that will support sporulation are key factors. 

The exotic, introduced organism P. ramorum has found a favorable environment 

and suitable hosts in the mixed-evergreen, redwood/tanoak, bishop pine, and tanoak 

forests of coastal California and southwest Oregon; in gardens, woodlands, plantations, and parks in the United Kingdom (DEFRA 2004); and in nurseries. 

The life cycle of P. ramorum is similar to that of other Phytophthora species. 

The pathogen produces sporangia on the surfaces of infected leaves and twigs 

of foliar hosts that can be splash-dispersed to neighboring hosts or driven longer 

distances by wind and rain. Phytophthora ramorum is also spread downstream 

of infested areas in rivers and streams, and can be carried in infested soil. Upon 

contact with a suitable host and environment, the sporangia germinate to produce 
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GENERAL TECHNICAL REPORT PSW-GTR-234

zoospores that encyst, penetrate the host, and initiate a new infection. Chlamydospores are readily produced in infected plant material and serve as resting 

structures in soil, allowing the pathogen to survive adverse conditions. Moisture is 

essential for survival and sporulation, and the duration, frequency, and timing of 

rain events during the winter months plays a key role in inoculum production. 

Knowledge of the disease cycle and the environmental requirements of P. 

ramorum to complete each stage of the cycle are needed to effectively manage the 

diseases the pathogen causes. Some examples of potential management actions 

based on the disease cycle of P. ramorum are summarized in Rizzo and others 

(2005). For instance, the findings that P. ramorum inoculum survives in soil has led 

to recommendations to avoid movement of soil from infested to uninfested areas. 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Chapter 4: Modeling Disease 

Distribution and Spatial-Temporal 

Patterns of Mortality

Introduction 

This chapter discusses the development and use of models to predict areas at risk 

for Phytophthora ramorum occurrence, and summarizes the literature on modeling 

of the spatial-temporal aspects of the disease.

Risk Models

Disease models are used to predict and describe the interaction between the 

environmental, host, and pathogen variables that result in disease. The variables 

used are based on laboratory and field data regarding the host and the pathogen, as 

well as on disease spatial and temporal variability (http://www.ipm.ucdavis.edu/

DISEASE/DATABASE/diseasemodeldatabase.html). Using climate and P. ramorum host distribution data, computer models that predict areas at risk for pathogen 

occurrence have been developed. These risk models are valuable tools used by 

researchers, managers, and policymakers to assist in early detection, survey, 

prevention, and regulatory policy decisions.

Regional Risk Models

California—

Models predicting the potential distribution of P. ramorum in California have been 

developed. Meentemeyer and others (2004) developed an expert-knowledge-driven, 

rule-based geographic information system (GIS) infection risk model (a rule-based 

model uses research data and expert input, rather than statistical inference, to 

determine the importance of predictor variables), to predict the risk of spread and 

establishment of P. ramorum in California based on plant host susceptibility and 

weather variables (precipitation, relative humidity, maximum temperature, and 

minimum temperature). Host distribution and monthly weather conditions were 

analyzed in a GIS to generate risk rankings per variable and per month. Spread 

risk predictions were then generated by combining the variables over the 6-month 

pathogen reproductive period (December through May) and averaged to generate 

the risk map (fig. 2). The model characterized the climate of coastal California—

from Del Norte County in the north to San Luis Obispo County in the south—and 

the western slopes of the northern Sierra Nevada in Butte and Yuba Counties, as 
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GENERAL TECHNICAL REPORT PSW-GTR-234

Very high

High

Moderate

Low

Very low

County boundaries

Large water bodies

SOD risk

Figure 2—Six-month average (December–May) predicted spread risk map for Phytophthora ramorum, cause of 

sudden oak death (SOD), in California (Meentemeyer and others 2004).
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

moderately to highly suitable for establishment and spread of P. ramorum from 

December to May.

Guo and others (2005) used and compared one-class and two-class support 

vector machine (SVM) techniques1 to predict the potential distribution of P. ramorum in California. Because the data often required by other methods to map the 

predicted spread of a disease may be unknown with a recently introduced pathogen 

such as P. ramorum, the authors compared one-class SVM models (using presenceonly data) and two-class SVM models (using both presence and pseudo-absence 

data). Fourteen variables (seasonality of climatic variables such as temperature, 

precipitation, and solar radiation—which are considered key to limiting P. ramorum—as well as distance to main roads and distance to edges of patches of hosts) 

were used to predict the potential distribution of P. ramorum in California. The 

one-class SVM predicted a greater risk area (fig. 3), including much of the foothills 

of the central Sierra Nevada, and along the coast in Humboldt County to the north 

and Los Angeles County to the south. The authors suggested that one-class SVMs 

are computationally more efficient (no need to generate pseudo-absence data) than 

two-class models, and are more applicable in the case of a new invasive species 

where absence data are not available.

1 Techniques for separating data points into classes. Support vector machines derive 

nonlinear boundaries to optimally separate clouds of points.

Hosts for P. ramorum

Areas predicted to be

at risk for SOD

County boundaries

Kilometers

Figure 3—Predicted area of sudden oak death (SOD) risk in California. Mapped results from (A) one-class support 

vector machines (SVMs) and (B) two-class SVMs (Guo and others 2005).
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GENERAL TECHNICAL REPORT PSW-GTR-234

Oregon—

For western Oregon, Václavík and others (2010) developed two GIS predictive 

models—based on weather and climate variability, host vegetation susceptibility 

and distribution, and dispersal—of P. ramorum establishment and spread risk 

for use in target monitoring and eradication activities. The first was a heuristic 

(rule-based) model, using a multicriteria evaluation (MCE) method, to identify 

the areas at potential risk of pathogen establishment and spread. The resulting risk 

map displayed a distinct geographical pattern of P. ramorum establishment and 

spread risk in western Oregon based on the influence of host species abundance and 

climate parameters (fig. 4). Although large areas had low to very low P. ramorum

risk in the eastern part of the area (owing to low host availability and unfavorable 

climate conditions), vast areas of forest across the western region of the state appear 

to be susceptible. The forests at greatest risk of disease spread are concentrated in 

southwestern Oregon where the highest densities of susceptible host species exist, 

in particular tanoak (Lithocarpus densiflorus (Hook. & Arn.) Rehd.).

For the second model, the authors used maximum entropy (MAXENT) to 

predict the current distribution of P. ramorum infections within the 2008 quarantine area in Oregon. Probability of infection was calibrated based on the correlation 

Very low risk

Low risk

Moderate risk

High risk

Very high risk

Figure 4—Predicted risk map of Phytophthora ramorum potential risk of establishment and spread in western Oregon (Václavík 

and others 2010).
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

between 500 field observations of disease occurrence and predictor variables 

including climate variability, host susceptibility and abundance, topographic variables, and a dispersal constraint. The model indicated that likelihood of the disease 

is positively associated with temperature and precipitation, and negatively associated with elevation and potential solar radiation. Tanoak abundance was strongly 

associated with disease presence.

National Risk Models 

The U.S. Department of Agriculture, Forest Service (USDA FS) developed a 

national risk map for P. ramorum in 2002 as part of the sample design for a national 

SOD detection survey (Smith and others 2002, USDA FS 2004). Variables used 

included (1) distribution of hosts known or likely to be susceptible to the pathogen, 

(2) climatic conditions adequate for survival and propagation of the pathogen, and 

(3) pathways for introduction of the disease outside the currently infested region. 

The resulting map consisted of hexagons indicating three levels of risk (high, 

moderate, low; the larger the hexagon, the less the risk) covering the conterminous 

United States (fig. 5).

Figure 5—U.S. Department of Agriculture, Forest Service national sudden oak death (SOD) risk map, 2002 

(Smith and others 2002).
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GENERAL TECHNICAL REPORT PSW-GTR-234

An updated national risk map was created (Koch and Smith 2008) by incorporating current data and approaches (recent host information, daily rather than 

monthly weather data, exclusion of areas where the minimum temperature was 

below 0 oC for 150 or more days, and consideration that P. ramorum could escape 

from ornamental plantings in residential landscapes into natural forests) to better 

depict principal factors of P. ramorum risk. The resulting map (fig. 6) showed an 

expansion of risk areas in the Southeastern United States and a shifting of risk in 

portions of mid-Atlantic and south-Midwest States from moderate to low.

Magarey and others (2006) used the North Carolina State University/Animal 

and Plant Health Inspection Service (APHIS) Plant Pest Forecast System (NAPPFAST) (Borchert and Magarey 2004) to construct a climate and host risk map for 

P. ramorum (fig. 7). The map was based on an assumption that P. ramorum occurrence would be climatically limited by temperature and moisture requirements. 

They used 10-year historical climate data. Initially, the daily combination of minimum temperature, optimum temperature, maximum temperature, and total hours 

per day of leaf wetness was used to estimate the annual number of days suitable for 

infection. A second modeling effort examined the effects of soil temperatures less 

than -25 °C, which reduce survival of P. ramorum sporangia and chlamydospores 

in laboratory tests (DEFRA 2005b). The cold temperature exclusion reduced the 

Ordinal Risk

High

Moderate

Low

Figure 6—Revised U.S. Department of Agriculture, Forest Service national sudden oak death risk map, 

2008 (Koch and Smith 2008).
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

northern extent of risk from the pathogen. Magarey and others (2008) then incorporated understory sporulator hosts (seven Ericaceae hosts of P. ramorum) into the 

model to further refine the at-risk infection areas (fig. 7).

Kelly and others (2007) compared and evaluated the performance of five spatial 

risk models (rule-based expert-driven GIS overlay, logistic regression [LR], classification and regression trees [CART], genetic algorithms [GA], and SVMs) generated 

from common input parameters to map risk from P. ramorum across the conterminous United States (fig. 8). All models were consistent in their prediction of some 

SOD risk in coastal California, Oregon, and Washington; in the northern foothills 

of the Sierra Nevada in California; in an east-west-oriented band including eastern 

Oklahoma, central Arkansas, Tennessee, Kentucky, northern Mississippi, Alabama, 

Georgia, and South Carolina, parts of central North Carolina, eastern Virginia, 

Delaware, and Maryland.

Figure 7—The chance of occurrence based upon at least 60 favorable days for infection by Phytophthora ramorum, hardwood hosts, understory sporulator hosts, and -25 °C lethal soil temperature exclusion (DEFRA 2005b; Fowler and others 

2006; Margarey and others 2007, 2008).
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GENERAL TECHNICAL REPORT PSW-GTR-234

Figure 8—Risk for sudden oak death (SOD) in the conterminous United States from five spatially referenced models: 

(a) rule-based, (b) logistic regression, (c) classification tree, (d) genetic algorithm, and (e) support vector machine (Kelly 

and others 2006, 2007).

The results from the five models were combined together to create a final map 

based on model agreement (fig. 9) (Kelly and others 2007).

A national rule-based and expert knowledge model to characterize suitable 

habitat for P. ramorum across the United States was developed by Venette and 

Cohen (2006). With the assumption that adequate inoculum and susceptible hosts 

are uniformly present across the contiguous United States and the use of CLIMEX 

software, the model focused on climate as the limiting factor in establishment of the 

disease. Model outputs (fig. 10) identified many areas within the United States that 

do not have a climate suitable for the establishment of P. ramorum, including most 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Risk for SOD

Low

Medium

High

Figure 9—Risk for sudden oak death (SOD) in the conterminous United States based on agreement between five 

spatially referenced models (Kelly and others 2007).

EI assuming no stress

0 (Unsuitable)

1-10 (Marginal)

11-25 (Favorable)

26-54 (Very favorable)

No data

Figure 10—Predicted climatic suitability for establishment of Phytophthora ramorum in the contiguous United 

States based on the ecoclimatic index (EI) from CLIMEX excluding environmental stresses (Venette and Cohen 

2006).
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GENERAL TECHNICAL REPORT PSW-GTR-234

of the Great Lakes, Plains, or Intermountain States. In addition to the Pacific Coast, 

climate is relatively more suitable for establishment in Southeastern, Northeastern, 

and Mid-Atlantic States.

The risk map produced by Venette and Cohen (2006) was consistent and in 

general agreement with other national risk models for P. ramorum, providing a 

degree of confidence in the conclusions from the models. 

In 2005, the USDA Animal and Plant Health Inspection Service (APHIS) compared eight national-scale risk models for P. ramorum. A summary of the comparisons is presented at http://nature.berkeley.edu/comtf/pdf/P%20ramorum%20v5%20

BRS%20rev.pdf. The models were subdivided into two groups: those that use P. 

ramorum observations and those that do not. In general, models that use P. ramorum observations predicted a more restricted distribution than those that do not. 

The models were generally consistent in showing a national pattern of high risk in 

the coastal Northwest and the central Appalachian Mountains, and a low risk in the 

Great Plains. The models differed in predicting the degree of risk in the Northeast, 

coastal California, parts of the Southeast and the northern Midwest. The greatest 

uncertainties among the models were the extent of the northern boundary of risk 

east of the Rocky Mountains and the degree of risk in the Southeast. The review 

paper recommends comparing the output from several models rather than using a 

single model for decisionmaking.

North American Temperature Model

McKenney and others (n.d.) presented a map based on North American continentwide extreme minimum temperature models (fig. 11). Based on a Department 

for Environment, Food and Rural Affairs (DEFRA) report that indicated all P. 

ramorum spores are killed after 4 hours exposure to -25 oC (DEFRA 2005b), the 

map may be useful in indicating climate limitations on potential distribution of 

the pathogen. Although useful in identifying possible environmental limits, a 

map based on minimum temperature only does not take into account other hostpathogen-environment interactions involved in disease introduction (McKenney 

and others 2003).

Europe

The European risk analysis for P. ramorum (Sansford and others 2009) presents 

various climatic models for predicting presence of the pathogen in Europe. A 

climate-based risk map for Europe, using the ranking system developed by Meentemeyer and others (2004) to predict potential P. ramorum distribution in California, 

is presented in fig. 12. The model uses climatic parameters that favor P. ramorum, 

with scores, ranks, and weights assigned to precipitation, maximum temperature, 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Figure 11—Extreme minimum temperature models for North America (McKenney and others, n.d.).

Risk ranking

Figure 12—Phytophthora ramorum risk ranking model for Europe, based on Meentemeyer and others (2004).
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relative humidity, and minimum temperature. However, because of a lack of 

high-resolution data for host distribution and host associations, it does not incorporate the host-species index of Meentemeyer and others (2004). The most suitable 

climatic locations for establishment are northern Portugal, northwestern Spain, 

the southern tip of Spain, the Adriatic coast of the Balkan peninsula, southwestern 

France, northwest France (Brittany), northern coastal Spain, southern Turkey, 

western United Kingdom and southwest Ireland. Note that those areas that are 

climatically favorable are only at risk where there are susceptible host plants that 

are capable of supporting P. ramorum sporulation.

International Risk Model

An international risk model for P. ramorum was created using NAPPFAST 

(Magarey and other 2006, 2008) (fig. 13), and the Intergovernmental Panel on 

Climate Change data set (historical climate data for the last 10 years). The data set 

contains variables describing average temperature, precipitation, humidity, and 

Frequency of occurrence (in 10 years)

Figure 13—The North Carolina State University/APHIS Plant Pest Forecast System (NAPPFAST) Intergovernmental Panel on Climate Change (IPCC) model for Phytophthora ramorum assuming at least 2 favorable months 

(Magarey and others 2006).
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

cloud cover. The model was based on a favorable month requiring average maximum monthly temperature to be less than 28 °C, average minimum temperature to 

be greater than 3 °C and at least 10 days with precipitation. Although Margarey and 

others pointed out that the model overestimates potential areas of pathogen occurrence because minimum precipitation data are not included, they suggested that the 

model may be of use in searching for the origin of the pathogen.

Refinement of the regional, national, and international risk models developed 

for P. ramorum will occur as host range, environmental factors favoring spread 

and establishment, and the effects of spatial and temporal variables affecting the 

pathogen are better understood (Rizzo 2006). The differences that exist among 

the risk models point out uncertainties and the need for additional information on 

suitable environmental niches for the pathogen.

Modeling Spatial-Temporal Patterns of Disease 

Distribution and Spread

Kelly and Meentemeyer (2002) and Liu and others (2007) used remote sensing 

and spatial analysis to quantify the clustering of overstory mortality associated 

with SOD across large scales. High-resolution imagery in combination with GIS 

and spatial modeling was used by Kelly and Meentemeyer (2002) to determine the 

presence and scale of oak mortality clustering over a 2-year period (2000 and 2001) 

at a location in Marin County (China Camp State Park), California. They found 

clustering patterns between 100 and 300 m. They also developed a classification 

tree model to predict spatial patterns of risk for oak mortality based on landscape 

variables. Factors correlated with oak mortality included proximity to forest edge, 

topographic moisture index, proximity to trails, abundance of California bay laurel 

(Umbellularia californica (Hook. & Arn.) Nutt.), and potential summer solar radiation. Their results suggested that forest structure was an important risk factor in 

spatial pattern and spread of the disease.

Liu and others (2007) analyzed the spatial-temporal patterns of overstory oak 

tree mortality at the same Marin County location (China Camp State Park) over a 

4-year period using point patterns mapped from high-spatial-resolution remotely 

sensed imagery. Univariate spatial-point pattern analyses showed that the point 

patterns of dead oak trees are significantly clustered at different scales and spatial 

extents through time; and that both the extent and the scale of the clustering patterns decrease with time. Multivariate spatial-point pattern analyses showed that 

newly dead oak trees tend to be located within 300 m of dead oak trees, and that a 

strong spatial association exists between oak tree mortality and California bay trees 

within 150 m.
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Because remote sensing used by Kelly and Meentemeyer (2002) and Liu and 

others (2007) does not capture understory or tree-specific symptomology, Kelly and 

others (2008) used two-dimensional transect data to cover large areas and capture 

vegetation detail and spatial location. Kelly and others (2008) investigated the 

spatial-temporal patterns of symptoms associated with SOD across landscape scales 

(hundreds of meters) at China Camp State Park. Using two-dimensional spatial 

analysis tools with data gathered in point-centered-quarter format in 2001 and 

2004 at the park, they quantified the clustering of dead trees across the landscape 

and then investigated the relationship between disease symptoms and dead trees 

through space and time. The work provided an estimate of the density of symptomatic trees at different levels of disease across a forest landscape affected by P. ramorum. Dead trees were strongly clustered at smaller scales (about 300 m) in 2001, but 

after 3 years (2004), the clustering was less pronounced despite an increase in dead 

crowns. These patterns supported those found using remotely sensed data across 

the park (Guo and others 2007, Kelly and Meentemeyer 2002, Kelly and others 

2004, Liu and others 2006), where clusters of overstory tree mortality of 200 to 400 

m across were found. Results showed that bleeding trees occur early in clusters and 

separate from existing dead trees, suggesting a new cohort of infected trees; that 

beetle-attacked trees exist throughout the forest and are not well correlated with 

overstory mortality; and that the saprophytic sap rotting fungus Hypoxylon [Annulohypoxylon] thouarsianum is strongly related to tree mortality through time (Kelly 

and others 2008).

In a study at Sonoma Mountain, Sonoma County, California, Condeso and 

Meentemeyer (2007) showed that disease severity (derived by counting the number 

of symptomatic leaves on each California bay laurel stem greater than 2 cm in 

diameter at 1.4 m for 90 seconds), was greater in forests with high connectivity 

and with high abundance of host species. More connected forests had more disease 

than smaller and more isolated forests, suggesting to the authors that forest fragmentation may keep inoculum levels low and reduce pathogen spread. They also 

demonstrated that, in the system they used, optimum microclimatic conditions for 

P. ramorum reproduction and growth are influenced more by elevation than by 

landscape pattern.

In a followup study, Meentemeyer and others (2008b) reported that altered forest structure and composition, probably largely owing to fire suppression, facilitated 

spread of P. ramorum. Using detailed aerial photography records between 1942 and 

2000 within a 150-m radius around 102 plots within a 275-km2

 area of northern 

California, they found that oak woodlands increased in area by 25 percent over the 

58-year period, while grasslands and chaparral (nonhost vegetation types) had both 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

significantly decreased. Path analysis showed that the woodland expansion resulted 

in larger forests with higher densities of the primary host trees (U. californica, 

Quercus agrifolia Née, Quercus kelloggii Newb.) and cooler understory conditions. 

The authors concluded that enlargement of woodlands and closure of canopy gaps 

facilitated the establishment of P. ramorum by increasing contagion of hosts and 

enhancing forest microclimate conditions. 

Although Meentemeyer and others (2004), Guo and others (2005), and Venette 

and Cohen (2006) mapped the potential spread risk of P. ramorum, Meentemeyer 

and others (2008a) provided a quantitative estimate of the pathogen’s realized 

spatial distribution. Meentemeyer and others (2008a) used niche modeling and 

dispersal estimation to examine the degree to which local habitat conditions vs. 

force of infection predict invasion by P. ramorum. Linear modeling indicated that 

the probability of invasion is limited by both niche constraints and dispersal. Probability of invasion was positively related to precipitation and temperature in the wet 

season and the presence of the inoculum-producing foliar host U. californica, and 

decreased exponentially with distance to inoculum sources. Model predictions suggested that future early detection sampling should concentrate on distances within 

33 km (the maximum distance an infection was detected) from a known source of 

inoculum.

In a preliminary abstract, Hunter and others (2008) described the development of a spatially explicit epidemic model that predicts susceptible-infectious (SI) 

transitions at discrete time steps using a geographic cellular automata approach. 

They developed a mathematical model that simulated spatial and temporal patterns 

of P. ramorum spread at large spatial scales. Using data (daily rainfall and temperature, host abundance and susceptibility, human population density, and pathogen 

dispersal characteristics) from field and laboratory studies, they parameterized 

the variables to develop a model that was implemented in GIS to simulate disease 

spread across California. The model predicted about 80 percent of the spatial variability in current patterns of spread of P. ramorum and identified numerous forest 

ecosystems at high risk of infestation.

Meentemeyer and others (2008c) quantified host mortality caused by P. ramorum across the Big Sur ecoregion using remote sensing (high-resolution aircraft 

imagery) in combination with regression models and field observations. Application 

of the regression models in a GIS estimated 235,678 standing dead trees in 2005 

and 12 650 m2

 of tree basal area removed from the ecoregion (79 366-ha study 

area), with 64 percent of mortality occurring in redwood-tanoak forests and 37 

percent in mixed-oak woodlands.
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GENERAL TECHNICAL REPORT PSW-GTR-234

The spread of P. ramorum in the nursery trade has been modeled using the 

concept of networks (a set of nodes connected by links). Nodes are the nurseries 

trading susceptible species, and links are shipments of those plants between nurseries. If nodes are connected to other nodes randomly (with a certain probability p), 

then the network is random. Scale-free networks are characterized by the presence 

of hubs, or super-connected individuals. Modeling of P. ramorum spread through 

nursery networks in England and Wales has demonstrated pathogen movement 

on a scale-free (compared with random) network, indicating that action at places 

of production (critical nodes) will help limit future spread (Jeger and others 2007, 

Pautasso and others 2008). 

A model framework useful to those concerned with the accidental introduction 

of P. ramorum into the Eastern United States from infected nursery plants was 

presented by McKelvey and others (2008). They are developing a spatial network 

model framework, using potential interstate nursery stock movements on a bipartite 

network. A Bayesian approach is used to model probabilities of transmission of 

P. ramorum from entry to destination nodes within the network. Probabilities of 

transmission of P. ramorum from source to destination nodes within the network 

are based on nursery stock flow volumes along the links connecting each origin/

destination pair. The objective is to identify locations throughout the United States 

that are most likely to receive nursery stock infected with P. ramorum. Such 

information would increase the efficiency of ongoing national survey programs for 

the pathogen. 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Chapter 5: Management and Control

Introduction

Although diseases caused by Phytophthora ramorum Werres, Cock, & Man in’t 

Veld have been studied only since about the year 2000, the literature abounds 

with results of numerous research and administrative study efforts to manage and 

control the pathogen. The existing literature is found in a wide array of publications 

(journals, popular articles, research summaries) and formats (printed articles, Webbased articles, abstracts, posters). The objective here is to summarize the literature 

on management and control of P. ramorum so that it will be available to researchers, managers, and publics concerned with the pathogen and the diseases it causes. 

The hope is that the increased availability of the literature will improve treatments 

and thus forest health. 

Disease Management Principles

Basically, disease management involves prevention—any action taken before the 

host is infected to protect it from disease, or suppression—an action taken against 

the pathogen after the host is infected. Several different systems have been used to 

group and discuss prevention and suppression strategies. Whetzel (1929) described 

four general disease control principles: exclusion, eradication, protection, and 

immunization (resistance). Although these principles have been expanded or altered 

to some extent over the years, they remain valid. Whetzel’s (1929) breakdown is 

used here to structure the literature on management and control of P. ramorum. The 

first two principles, exclusion and eradication, involve pathogen control; the second 

two, protection and resistance, deal primarily with plant defenses. Some actions 

may fall into more than one of the categories.

The four disease control principles can be summarized as follows:

Exclusion: Any strategy that attempts to prevent the introduction of a pathogen 

into an area where it is not yet present. Exclusion is aimed at preventing the introduction of inoculum, or reducing the amount of initial inoculum introduced, from 

outside sources.

Eradication: The strategies are aimed at eliminating or reducing a pathogen 

after it is introduced into an area, but before it has become well established or 

widely spread. Eradication involves strategies that eliminate, destroy, or inactivate 

the inoculum through sanitation, removal of reservoirs of inoculum, removal of 

hosts or alternate hosts, and other methods. 
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Protection: Protection strategies assume that the pathogen is present and 

that infection will occur without the intervention of protective measures. Protection prevents or reduces infection by means of a toxicant or some other barrier to 

infection. It establishes a barrier between the pathogen and the host plant or the 

susceptible part of the host plant. It is usually thought of as a chemical barrier such 

as a fungicide, bactericide, or nematicide, but it can also be a physical, spatial, or 

temporal barrier. 

Resistance: Resistance strategies use a host or hosts that are resistant to or 

tolerant of infection. Cultivars or varieties that reduce the rate of inoculum production, the rate of infection, or the rate of pathogen development are deployed. Use of 

disease-resistant plants can be an effective and environmentally sound method to 

manage plant diseases if plants of satisfactory quality and adapted to the growing 

region with adequate levels of durable resistance are available.

Early plant pathologists stated the principles of control in absolute terms, 

such as eliminate, exclude, and prevent. Today, we realize that absolute control to 

eliminate a pathogen is often not possible, but that management of the disease to 

acceptable levels is a more realistic goal.

Exclusion

Exclusion involves a combination of quarantines or regulations and best management practices (BMPs) designed to prevent pathogen introduction. Phytophthora 

ramorum can be moved with infected plants, in water, in infested soil, and via wood 

or potentially other infected plant products (see chapter 3, “Inoculum Dispersal” 

section). There is, therefore, the need for regulations and BMPs to prevent spread.

Regulations

To reduce or eliminate P. ramorum spread, regulatory actions are being implemented and enforced in countries worldwide. The U.S. Department of Agriculture, 

Animal and Plant Health Inspection Service (USDA APHIS) issued a national 

strategic plan (USDA APHIS 2005b) that addresses the control and management 

of P. ramorum in cultivated and natural environments. The strategy’s first defense 

is exclusion, to prevent pathogen introduction and disease development in new 

areas. The primary objective of the national strategy is to “prohibit introduction, or 

significantly reduce the rate of introduction or reintroduction, of P. ramorum, into 

presently noninfested regions of the United States, and to manage presently infested 

nursery systems, forests, and urban landscapes to minimize and mitigate damage.” 

Numerous countries have placed restrictions on the movement of affected plants 

and plant parts from the United States (Purdue University Center for Environmental 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

and Regulatory Information Systems Export Certification Project 2007, Rizzo and 

Garbelotto 2003). Worldwide, the European Union pest risk analysis for P. ramorum (Sansford and others 2009) lists 68 countries for which P. ramorum is either on 

their lists of regulated pests or mentioned in their legislation. 

Federal regulations in the United States and Canada—

In the United States, USDA APHIS is responsible for promulgating and enforcing 

interstate and international plant quarantine measures. In addition, state agencies 

regulate within-state quarantines. The first P. ramorum quarantine was issued in 

2001 by the state of Oregon. It banned host plants and host plant products coming 

from California unless they had been treated (Frankel 2008). Canada issued a similar quarantine the same year, prohibiting the import of nursery stock and unmanufactured, nonpropagative host material (such as logs and mulch) from areas where 

P. ramorum had been found (Frankel 2008). Then, on 17 May 2001, the California 

Department of Food and Agriculture (CDFA) issued emergency regulations that 

restricted the export of diseased oak products and rhododendrons from each of the 

seven infested counties (Frankel 2008). The USDA APHIS followed by issuing an 

interim federal regulation (7 CFR Part 301) in February 2002 for domestic interstate 

movement of P. ramorum host material from the known infested California counties. The regulation 7 CFR Part 301 was amended in 2007 (USDA APHIS 2007a).

In January 2005, a new federal order (Emergency Federal Order Restricting 

Movement of Nursery Stock From California, Oregon, and Washington Nurseries 

December 21, 2004, USDA) was issued. The order (USDA APHIS 2005a) regulates 

interstate movement of nursery stock from uninfested areas in California, Oregon, 

and Washington. Under the federal order, all nurseries with host or associated host 

plants on site must be inspected and found free of P. ramorum before they can ship 

nursery stock interstate (Frankel 2008). If P. ramorum is detected at a nursery, the 

Confirmed Nursery Protocol (USDA APHIS 2004) requiring the destruction of the 

infested plants and all other host and associated host plants in the contiguous block 

as the infected plant is implemented. The block is considered contiguous until there 

is a 2-m break of either no plants or no hosts or associated host plants. The site is 

delimited, and all host plants are held and monitored for 90 days. The nursery will 

continue to be monitored for at least 2 years. The protocols, regulated articles and 

scope of the U.S. federal regulations may be found on the USDA APHIS P. ramorum Web site (http://www.aphis.usda.gov/plant_health/plant_pest_info/pram/). An 

examination of nursery survey data for the Western States from 2004 to 2006 found 

that the number of P. ramorum-infested nurseries dropped by more than 50 percent 

(from 110 nurseries to 50) (Suslow 2008a). See table 2 in chapter 2 for U.S. nursery 

detections by year. In addition to the effectiveness of the 2005 federal order, the 
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drop was attributed to training of nursery growers and to implementation of nursery 

research findings (Suslow 2008a). 

Regulations and quarantines are continuously updated to reflect new findings. 

Consult the USDA APHIS PPQ (Plant Pest and Quarantine) P. ramorum Web site 

(http://www.aphis.usda.gov/plant_health/plant_pest_info/pram/regulations.shtml) 

for up-to-date information, or see the www.suddenoakdeath.org Web site for regulations and regulatory updates in the United States.

A residential protocol is also provided by APHIS. The residential protocol 

(USDA APHIS 2009) specifies actions that are to be taken when a positive P. 

ramorum infection is confirmed in plantings in residential or commercial landscape 

settings. The objective is pathogen eradication from the site.

European Union/international regulations—

In November 2002, the European Union adopted emergency measures to prevent 

the introduction and movement of P. ramorum into and within the EU nations. Legislation (2002/757/EC) to control the introduction of susceptible hosts into the European Community, in particular, the import of susceptible plants and plant products 

from the United States, was enacted (OJEC 2002). For export of susceptible plants 

from the United States to member countries in the European Union, plants must 

originate from a P. ramorum-free area or from a place of production that has been 

inspected by U.S. authorities and found free from symptoms. The movement of 

Rhododendron, Viburnum, and Camellia (the main hosts of P. ramorum in Europe; 

Camellia was added in 2004) within the European Union are controlled via "plant 

passports," certificates verifying that the plants have had the required statutory 

inspections and have been found free from quarantine pests (including P. ramorum). The legislation also calls for all EU member states to undertake surveys for P. 

ramorum and disseminate the results. If P. ramorum is found, then all susceptible 

plants within 2 m are destroyed. Any additional susceptible plants within 10 m are 

held for a period of 3 months’ active growth, with at least two additional inspections before being released. The rest of the facility is intensively reinspected before 

allowing plants to be moved. The legislation was amended in 2004 (Commission of 

European Communities 2004) to incorporate Camellia as a host requiring a plant 

passport, and in 2007 (http://www.eppo.org/ABOUT_EPPO/EPPO_MEMBERS/

phytoreg/eu_texts/2007-201-EC-e.pdf) (OJEC 2007) to add measures relating to 

destruction of associated growing media and plant debris and other appropriate 

phytosanitary measures applied to the growing surface. An analysis of the effect 

of these measures on the prevalence of P. ramorum during the period 2004 to 2006 

(Slawson and others 2008) showed a reduction in the percentage of inspections 

positive for P. ramorum and a reduction in the number of outbreaks at nurseries; 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

however, the continued pathogen findings indicated that the phytosanitary measures 

have not been completely effective. 

Best Management Practices

Best management practices are methods, measures, practices, or procedures that 

have been determined to be effective means of preventing or reducing adverse 

effects. Through experience, research, and knowledge of the disease cycle of P. 

ramorum, BMPs to prevent or reduce pathogen spread have been compiled. Many 

of the practices are meant to exclude P. ramorum from noninfested areas by preventing or reducing the risk of spread. They are usually most effective when applied 

as a system rather than as individual practices.

BMPs in wildlands and urban-interface zones—

Numerous publications outline BMPs to prevent or reduce the spread of P. ramorum. These BMPs provide guidelines to prevent or minimize the introduction and 

subsequent spread of P. ramorum by limiting movement of host material or infested 

soil. The California Oak Mortality Task Force (COMTF) at www.suddenoakdeath.

org has compiled BMPs for a number of activities and user groups on wildlands and 

in urban-interface zones. They include guidelines for forestry, recreational users, 

forest collectors, arborists, homeowners, firefighters, tribal plant gatherers, and 

Christmas tree growers (California Oak Mortality Task Force 2004a, 2004b, 2004c, 

2004d, 2005, 2006a, 2006b, 2006c). In 2002, the Management Committee of the 

COMTF compiled BMPs for zone of infestation-regulated areas (California Oak 

Mortality Task Force 2002); measures to prevent spread of the pathogen during tree 

removal or pruning in regulated areas, and measures to minimize the movement of 

host material and soil from infested areas are presented. 

In the United Kingdom, a best practice guide for woodlands, parks, and gardens 

(P. ramorum—A Practical Guide for Established Parks & Gardens, Amenity Landscape and Woodland Areas) is available from the Department for Environment, 

Food and Rural Affairs (DEFRA) Web site at: http://www.fera.defra.gov.uk/plants/

publications/plantHealth/documents/pramparks.pdf.

BMPs in nurseries—

The management of P. ramorum in nurseries is based on minimizing the risk of 

introduction and preventing pathogen establishment. Numerous BMPs or guidelines 

on P. ramorum in nurseries are available. The guidelines are designed to encourage general cleanliness standards to minimize introduction and establishment of 

the pathogen. On December 21, 2004, the USDA APHIS adopted an Executive 

order that requires all nurseries in California, Oregon, and Washington that export 

nursery stock interstate to be surveyed for P. ramorum. The Oregon Department of 
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Agriculture adopted a similar regulation shortly thereafter (Phytophthora ramorum

Regulated Area for Nursery Stock). Based on these regulations, guidelines were 

developed in cooperation with the California Association of Nurseries and Garden 

Centers, the Oregon Association of Nurseries, the Washington Nursery and Landscape Association, Oregon State University, the Oregon Department of Agriculture, 

and the Washington State Department of Agriculture (Parke 2005). The BMPs 

for California nurseries, developed by the Nursery Committee of the COMTF 

(Suslow and others 2005) are divided into two categories: exclusion/prevention, and 

monitoring. Guidelines for Oregon nurseries (Parke and others 2003), Washington 

nurseries (Parke and others 2004), and California nurseries (Tjosvold and others 

2005) have been published. The guidelines are continuously updated as new information becomes available. 

A national working group, convened by The Horticultural Research Institute 

(HRI), the research arm of the American Nursery & Landscape Association 

(ANLA), developed a menu of nationally applicable BMPs for P. ramorum in 

nurseries. The group comprised diverse representatives from the nursery industry 

and key technical and research experts from the USDA Agricultural Research 

Service (ARS), the USDA APHIS, the Cooperative State Research Education and 

Extension Service (CSREES) and representatives of state Departments of Agriculture through the National Plant Board (NPB). The national working group evaluated 

and fine-tuned existing BMP plans from California, Oregon, and other regions. The 

product (Voluntary Nursery Industry Best Management Practices for Phytophthora 

ramorum—Introduction or Establishment in Nursery Operations Version 1.0) is 

available at http://www.hriresearch.org/docs/Publications/HRI%20Publications/

VoluntaryIndustryBestManagementPracticesPramorumweb1.pdf. The publication 

contains biosecurity guidelines, created by and for nursery growers, to reduce the 

risks associated with P. ramorum. The control of the pathogen is based on the insertion of multiple hurdles to prevent the introduction of the pathogen into nursery 

operations (Suslow 2008b).

The Oregon Department of Agriculture (ODA) has developed a Grower 

Assisted Inspection Program (GAIP) to help reduce the risk of nursery plants from 

becoming infected with P. ramorum. The objective of the GAIP is to assist nurseries to self monitor for Phytophthora species and mitigate pathogen problems using 

appropriate management practices. The program uses the best cultural practices 

(BCP) developed by researchers at Oregon State University for their online Phytophthora course. Standard operating procedures, structured from the BCP and 

best available science with modifications specific to each nursery, are used as 

appropriate. (http://www.oregon.gov/ODA/PLANT/NURSERY/gaip.shtml). Oregon 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

State University applied an approach based on Hazard Analysis of Critical Control 

Points (HACCP) for systematically detecting sources of Phytophthora contamination in four Oregon nurseries. The goal was to adapt the HACCP approach to 

identify critical control points (CCPs) for Phytophthora contamination in commercial nursery production systems. Critical control points are the best points, steps, 

or procedures at which significant hazards of contamination can be prevented or 

reduced to minimum hazard. Critical control points identified in the nurseries were 

(1) placement of healthy container-grown plants on contaminated soil/gravel substrates (all nurseries), (2) use of contaminated irrigation water (nurseries A and C 

only), and (3) use of contaminated used pots (all nurseries) (Parke and others 2010a).

Oregon State University Extended Campus (Ecampus) developed an online 

training course for the management of Phytophthora in nurseries (Parke and others 

2010b). The “Phytophthora Online Course: Training for Nursery Growers” provides 

access to nursery personnel and the public. The course includes three modules: biology, symptoms, and diagnosis; disease management; and Phytophthora ramorum. 

The course, accessed at (http://ecampus.oregonstate.edu/phytophthora), is available 

in Spanish as well as English.

The first national U.S. nursery site for invasive species research is being established in Marin County, California. The site, The National Ornamentals Research 

Site at Dominican University of California (NORS-DUC), is a secure site modeled 

to reflect a nursery for the purpose of performing studies on nursery stock in a “real 

world” environment while ensuring high-level safeguards to prevent the escape of 

plant pests. Initial studies will focus on understanding and controlling the longrange spread of P. ramorum through infested nursery stock shipments.

The British Columbia Nursery and Landscape Association has developed a P. 

ramorum certification program for nursery growers, silviculture, and floriculture 

industries (British Columbia Nursery and Landscape Association 2005). The 

objective is to minimize the risk of importing and moving the pathogen in the 

province. The program includes mandatory sampling and testing for P. ramorum, 

workshops for nursery staff, implementation of BMPs, and an audit by an independent organization. In the United Kingdom, a Practical Guide for the Nursery and 

Garden Centre Industry has been produced (http://www.fera.defra.gov.uk/plants/

publications/plantHealth/documents/pramnurs.pdf).

Eradication

If the disease is caught early enough, eradication is the current USDA policy to 

respond to new isolated occurrences of P. ramorum. Eradication efforts may be 

applied to large geographic areas, to smaller areas such as forest stands or nurseries, 
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or to individual host plants. Efforts to eliminate, destroy, or reduce inoculum, 

including sanitation efforts, can be included in eradication strategies. Eradication of 

any disease can only be successful if the pathogen is detected early and its distribution is limited. If eradication is not feasible, then attempts to control, manage, and 

mitigate impacts are considered. 

From Forests 

Eradication efforts in Oregon—

In July 2001, P. ramorum was discovered at nine disease centers in mixed tanoak 

(Lithocarpus densiflorus (Hook. & Arn.) Rehd.)/Douglas-fir (Pseudotsuga menziesii 

(Mirb.) Franco) forests near Brookings, Oregon (Goheen and others 2002b). Aerial 

photos of the area indicated that the pathogen had been present at one of the sites 

since about 1997. The pathogen was isolated from stem cankers on tanoak and from 

foliage and shoots of native Rhododendron and Vaccinium. All lands within 1.6 km 

of the disease centers, an approximately 2331-ha area, were subjected to Oregon 

and APHIS quarantines that prohibited the transport of host materials. Since the 

fall of 2001, state and federal agencies have attempted to eradicate P. ramorum

from those infested sites by cutting and burning all infected host plants and a buffer 

of adjacent apparently uninfected plants (Goheen and others 2004; Hansen and 

Sutton 2006; Kanaskie and others 2004, 2010a). The Oregon program now consists 

of early detection, delimitation of infested areas, treatment, research and monitoring, and host reduction in areas of probable disease spread. Following treatment, 

sites are monitored by baiting of streams and rainwater with leaves of tanoak and 

rhododendron, baiting of soils with pear fruits and tanoak and rhododendron leaves, 

and examining sprouting host plants for infection (Hansen and Sutton 2006). 

Between 2001 and 2008, more than 971 ha were treated at a cost of over $4 million 

(Kanaskie and others 2009). 

During the first 4 years of the eradication effort, the number of new infested 

sites and infected trees remained steady or decreased each year, indicating modest success at containment and eradication (fig. 14). In 2005, the number of new 

infected trees and the area infested began increasing. Delays in completing treatments and consecutive years of unusually wet spring and early summer weather 

contributed to spread of the disease, resulting in expansion of the quarantine zone 

from 6734 ha to 41 956 ha in 2008 (Kanaskie and others 2008a, 2010a).

Results of the Oregon program indicate modest to moderate success at eradication and good success at containment of the pathogen to a relatively small area, 

thereby reducing damage to forests and minimizing the economic impact of quarantine regulations (Kanaskie and others 2006b, 2008a, 2010a; Goheen and others 

2010). 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Efforts in northern California to slow the spread—

In contrast to the eradication efforts in Oregon forests, the strategies in California 

forests have been, by necessity, aimed not at elimination, but at efforts to slow the 

spread. These efforts involve reducing inoculum through sanitation, removal of 

reservoirs of inoculum, and removal of hosts or alternate hosts.

An infestation of P. ramorum in an area of about 518 ha of coast redwood 

(Sequoia sempervirens (D. Don) Endl.) forests near the town of Redway in a 

residential setting in Humboldt County, California, was confirmed in July 2002. 

Because eradication was not feasible, efforts were made to slow the spread of the 

disease there. The area was treated in February 2004 by removing infested tanoaks 

(Valachovic and others 2006). Additional areas of tanoak mortality in riparian 

forest settings near Redway and nearby Garberville were confirmed later in 2004. 

Because clearcutting was not an option owing to adverse environmental impacts, 

the residential setting, and other considerations, removal of hosts, including California bay laurel (Umbellularia californica (Hook. & Arn.) Nutt.) and madrone (Arbutus menziesii Pursh), to reduce inoculum was tested at various sites (Valochovic and 

others 2008) as part of an overall management program. Experimental silvicultural 

control efforts over 48.6 ha were implemented in 2006. The treatments included 

California bay laurel and tanoak removal (sporulating hosts of P. ramorum) in 

combination with pile and broadcast burning (Valachovic and others 2008).

Efforts to manipulate forest stands by pruning, host removal, thinning, and 

other actions to reduce incidence and impact of P. ramorum are underway in 

0

20

40

60

80

100

120

140

160

180

Year

Acres or trees

2001 2002 2003 2004 2005 2006 2007 2008 2009

Infected tanoak

Infested acres

Figure 14—Sudden oak death trends in southern Curry County, Oregon, 2001 to 2009.
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several other California locations, including the Big Sur area. To reduce the spread 

of P. ramorum, infected and symptomatic tanoaks were removed in fall 2009 from 

MacKerricher State Park campground north of Fort Bragg in Mendocino County. 

The Park infestation, first identified in spring 2009, is the first known occurrence of 

the disease along the northern Mendocino coast. The objective was not eradication, 

but a proactive and precautionary measure intended to help reduce the spread of 

the pathogen by reducing inoculum. After the trees were cut, the boles, branches, 

and leaves were burned in an air curtain incinerator. Other projected management 

actions for the site include the use of Agri-Fos® on selected tanoaks surrounding the 

site, as well as planting of Bishop pine (Pinus muricata D. Don) seedlings as part 

of a site rehabilitation effort (see http://nature.berkeley.edu/comtf/pdf/Monthly%20

Reports/COMTF_Report_November_2009.pdf).

From European Woodlands, Parks, and Gardens 

In Europe, when P. ramorum is found in natural and seminatural environments, the 

official EU requirement is that appropriate measures be taken to at least contain the 

harmful organism. Measures used in the European Union include prohibition on 

the movement of infected plants and parts of plants, destruction by removing and 

burning or composting of the plant material, prevention of regrowth, and restricting 

access to the outbreak area (OJEC 2007). 

In the United Kingdom, measures that are applied to outbreaks in the seminatural or natural environment include (Sansford and Woodhall 2007): 

• Prohibition on movement of the infected plant and parts of the plant (e.g., 

must not be used for propagation purposes or foliage purposes).

• Destruction of infected plants and susceptible plants within an appropriate 

cordon sanitaire [quarantine line] and associated plant debris.

• Prevention of regrowth.

• For infected trees, required felling or pruning depending on the part of the 

tree infected and the extent of infection.

• Measures required to prevent reinfection at the site (e.g., prohibition on 

planting susceptible plants in contaminated soil, removal or sterilization of 

contaminated soil).

In the United Kingdom, significant rhododendron clearance programs have 

been completed and are ongoing. Through 2007, more than 60 ha of rhododendrons 

have been cleared from woodlands in each of Cornwall and south Wales. Measures 

applied at garden/woodland outbreaks are aimed at containment with a view toward 

eradication. Experiments in historical gardens have shown that completely removing infected rhododendrons and other foliar hosts can prevent new plant infections. 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

In one garden, no new plant infections have been recorded 4 years after all the 

significant numbers of infected plants were removed (Turner 2007a); even though it 

can still be detected in soil and water courses, these levels of contamination appear 

to be epidemiologically insignificant. In soil, the pathogen is most likely surviving 

as chlamydospores. This type of spore maintains the pathogen in the U.K. environment for at least 2 years. Removal of foliar hosts protects susceptible trees from 

infection. Pruning out infections from infected foliar hosts (Rhododendron) in the 

United Kingdom has not proven overly effective, even with the use of fungicides 

applied prior to pruning to help protect cut surfaces from reinfection (Sansford and 

others 2009). The U.K. government has provided £25 million over 5 years (2009 

through 2013) to help contain and eradicate P. ramorum and P. kernoviae in historical gardens, woodlands, heathlands, and from nurseries and retailers in England 

and Wales.

In the Netherlands, eradication of P. ramorum from an infested public green 

was attempted by cutting back all infected rhododendrons to 30 cm. As an experiment, the remaining parts of the plants were treated with thiophanate–methyl, 

glyphosate, or left untreated, and the removal of plant debris and humus or plant 

debris only was tested. The regrowth and occurrence of new infections were 

monitored (Aveskamp and others 2006). The pathogen survived in the sandy soil for 

at least 1 year, and cutting back the rhododendron shrubs to 30 cm was not sufficient to eradicate P. ramorum from the infested public green. Measures taken in the 

Netherlands therefore now focus on containment.

From Nurseries 

United States—

In U.S. nurseries, eradication of the pathogen is the primary objective of the 

USDA APHIS strategic plan (USDA APHIS 2005b). Through protocols for tracing 

infected plants and mitigating infested nurseries, P. ramorum may be eliminated 

from nursery stock. Successful eradication can be demonstrated through scientifically valid survey and sampling plans. The implementation of clean stock programs 

and best management practices for nurseries can ensure that nursery stock moving 

in commerce is free of P. ramorum. 

A study of the federal confirmed nursery protocol (USDA APHIS 2004), which 

outlined the destruction of infected nursery stock, safe disposal of contaminated 

containers and growing media, and subsequent testing of the remaining plants 

onsite, was conducted in Oregon during an attempt to eradicate the pathogen in 

imported, infected nursery stock (Osterbauer and others 2004). Phytophthora ramorum was not detected in plants at the nurseries after the destruction of the originally 
82

GENERAL TECHNICAL REPORT PSW-GTR-234

infected plant material. The confirmed nursery protocol has apparently been used 

successfully in many nurseries, with the failures attributed to instances where P. 

ramorum survived in soil.

Canada—

The Canadian Food Inspection Agency (CFIA) conducts annual surveys for P. 

ramorum and has in the past detected the presence of the pathogen on plants in a 

number of retail/wholesale nurseries in the southern coastal area of British Columbia. Of the 4,314 samples taken at 60 sites in the 2008 National Nursery Survey, 24 

were positive for P. ramorum. Samples originated from 9 retail nurseries and 12 

landscape sites (http://www.inspection.gc.ca/english/plaveg/pestrava/surv/sit2008e.

shtml#phyram). Detections are followed by immediate eradication efforts. Eradication protocols for propagative nurseries (http://www.inspection.gc.ca/english/

plaveg/hort/pi-010e.shtml) and retail nurseries (http://www.inspection.gc.ca/english/

plaveg/hort/pi-011e.shtml) confirmed with P. ramorum have been developed. When 

P. ramorum is found at a retail nursery, all plants found infected, all hosts within 4 

m of the infested plants, and all high-risk host plants (plants in the genera Camellia, Kalmia, Pieris, Rhododendron, and Viburnum) within the retail nursery are 

placed under quarantine. Following extensive sampling for the pathogen, all plants 

identified as infested as well as all host plants within 2 m of the infested plants 

are destroyed (CFIA 2009). Extensive surveys and trace-forward and trace-back 

activities are conducted to ensure the organism has been eliminated. When the 

CFIA detects a plant infested with P. ramorum and takes regulatory action—such 

as ordering disposal and treatments, or imposing restrictions or prohibitions—individuals or companies may apply for compensation under the “Phytophthora ramorum compensation regulations.” 

European Union—

Eradication is being attempted in the European Union by destroying all infected 

plants within a 2-m (6.6-ft) radius of a diseased plant and holding all susceptible 

plants within a 10-m (32.8-ft) radius plus any remaining plants from the same consignment as the diseased plants for further assessment (Sansford and others 2009, 

Slawson and others 2006). Release of these plants is allowed following two negative 

visual inspections during 3 months of active growth. 

The eradication and containment actions required against P. ramorum in EU 

nurseries are:

• Destruction by burning or deep burial (infected plants, susceptible plants 

within a 2-m radius of infected plants and associated plant debris).
83

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

• Disinfection of surfaces.

• Prohibition on movement of susceptible plants within a 10-m radius of 

infected plants and remaining plants in infested lot for at least 3 months.

• Prohibition on use of Phytophthora fungicides during the holding period.

• Advise the cessation of overhead irrigation. 

• Trace-back and trace-forward of related plant material. 

In the case of a finding at a nursery, the following is required as a minimum 

(Sansford and Woodhall 2007): 

• Destruction of infected plants and all susceptible plants within a 2-m radius 

of the infected plants (from May 2007 this will include the destruction of 

associated growing media and plant debris, plus appropriate phytosanitary 

measures applied to the growing surface). 

• A quarantine period of 3 months of active growth for all susceptible plants 

within 10 m of the infected plants and any remaining plants from the 

affected batch.

• For plants under quarantine, treatments that might suppress symptom 

development are prohibited during the quarantine period.

• For plants under quarantine, at least two official inspections must be carried 

out during the quarantine period.

• All other susceptible plants at the place of production should be subject to 

intensive official reinspection during this period (from May 2007, appropriate phytosanitary measures will have to be taken on the growing surface 

within a 2-m radius of infected plants).

Additional measures that have been taken by individual EU member states 

include (Sansford and Woodhall 2007):

• No treatment that could suppress symptoms should be applied during the 

quarantine period for all susceptible plants at the place of production. 

• Where the infected plant is soil-grown, no host plant may be grown in 

the same area or the area immediately surrounding an infected plant for 3 

years. 

• A survey of plants within a 500-m radius around an infected place of production. 

• After a finding, regular checks of all other susceptible plants at the place of 

production, including testing of plants and soil. 

• Hygiene measures for container-grown plants, disinfection/destruction of 

cloth, pots, and any other associated material. 
84

GENERAL TECHNICAL REPORT PSW-GTR-234

Slawson and others (2006) reported some success with eradication in the United 

Kingdom of 462 outbreaks (376 at nurseries and garden centers and 86 on managed 

and unmanaged land) recorded through December 2004; 82 percent were eradicated 

from nursery and retail facilities, and 27 percent were eradicated from managed and 

unmanaged lands. Modeling work has indicated that in the United Kingdom, the 

nursery trade has the characteristics of a scale-free network in which major nodes 

predominate (Pautasso and others 2008). Such a scale-free network lends itself to 

the current regulatory controls, which focus on plant passporting of key genera and 

wholesale producers. Conversely, removal of controls would potentially result in 

rapid epidemic spread throughout such a scale-free network. In the Netherlands, the 

EU actions to prevent the introduction and spread of P. ramorum appear to be successful in nurseries, but less so in woodland areas (Steeghs and de Gruyter 2006). 

Steeghs and de Gruyter (2006) suggested that because P. ramorum is known from 

about 25 to 30 field sites in the country, complete eradication would not be possible. 

In the United Kingdom, measures applied to outbreaks in the seminatural or natural 

environment continue to aim at containment with a view to eradication (Inman 

2009).

Heat Treatments

Various heat treatment experiments have been done to determine efficacy in eradicating P. ramorum from infested host material.

Effects of composting on pathogen viability—

Composting is considered an effective treatment option for sanitization of P. 

ramorum-infected plant material (Garbelotto 2003a). Swain and others (2002, 2006) 

demonstrated that composting effectively eliminates P. ramorum from green waste. 

In laboratory heat treatment tests, wood chips and cankered stems from coast live 

oak and infected California bay laurel leaves were all noninfectious after a 2-week 

exposure at 55 °C. These same types of infectious plant materials were also used 

in field composting trials using both windrow and forced-air methods. All plant 

material extracted from compost piles was free from P. ramorum after 2 weeks, 

based on isolation and polymerase chain reaction (PCR) assay. The absence of P. 

ramorum DNA led the authors to conclude that the pathogen was absent and not 

merely suppressed or dormant. Aveskamp and Wingelaar (2006) demonstrated that 

the tunnel-composting process (heating plant material to a minimum of 60 °C for 

at least 10 hours under controlled conditions, with hot air flowing through the plant 

debris during the process) eliminated P. ramorum from infected Rhododendron

leaves and shoots among Rhododendron plant debris.
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Plant material infested with P. ramorum and brought into composting facilities may present a contamination risk to users of finished compost (Swain and 

Garbelotto 2006). Isolating sources of fresh plant material from curing and finished 

compost at facilities producing compost for commercial sale or transport out of 

quarantined areas is necessary to eliminate contamination.

Effect of heat treatments on pathogen viability—

Harnik and others (2004) showed that P. ramorum is highly heat tolerant and could 

be reisolated from artificially inoculated California bay laurel leaves placed at 55 °C 

for up to 1 week. The pathogen was not recovered after 2 weeks at 55 °C. Because 

the prolonged heat treatments are impractical for bay leaves intended to be sold 

commercially as a spice, the authors developed a treatment involving a gradual and 

progressive heating process combined with the application of a moderate vacuum 

(0.133 kPa) that could be completed in 22 hours; the treatment eliminated the recovery of P. ramorum, and had no negative effect on the quality of the bay leaves.

Jennings (2006) reported that a 30-minute dry heat treatment at 60 °C was 

required to achieve complete kill of P. ramorum. However, rhododendron, viburnum, and camellia plants were completely killed after a 20-minute dry heat treatment at 55 °C. The authors found an adverse effect on P. ramorum infections using 

a longer treatment period (130 minutes at 45 °C) on detached leaves, but whole plant 

treatment was ineffective in controlling symptom development (Jennings 2006). 

Moist, steam heat is apparently more effective than dry heat. Linderman and Davis 

(2006c) recovered P. ramorum sporangia or chlamydospores from soilless potting 

media up to 6 months after being added. Aerated steam pasteurization at 50 °C or 

higher for 30 minutes was an effective means of eradicating P. ramorum as well 

as other pathogens from the infested media and contaminated containers without 

destroying the containers.

Conifer bark requires either fumigation or heat treatment at 56 °C for 30 minutes before it can enter the EU from non-European countries. Tubajika and others 

(2008) found that a treatment at 56 °C for 30 minutes might not be adequate to kill 

P. ramorum in wood of tanoak. However, the results were inconclusive, particularly 

because the detection of P. ramorum in the controls was low. Swain and others 

(2006) showed that a 1-hour exposure at 55 °C was required to no longer detect P. 

ramorum in wood chips and cankered stems of coast live oak.

Protection

Protection strategies—those that provide a chemical, physical, spatial, or temporal 

barrier to infection—are used when the pathogen is present and infection will likely 

occur without the intervention of protective measures. Most barriers are chemical.
86

GENERAL TECHNICAL REPORT PSW-GTR-234

Chemical

A range of pesticides are available for use on P. ramorum. These include protective/preventive fungicides (products that remain on the host surface, protecting it 

from infection for a period of time; they do not enter the plant tissue), and systemic/

curative fungicides (products that are absorbed into the plant and are fairly mobile 

within the plant; some have curative properties, i.e., the ability to stop infection 

progress). The mode of action of a fungicide can be fungicidal (kills the pathogen) 

or fungistatic (inhibits the growth of the pathogen).

Treatment of oaks and tanoak, bark applications—

It was recognized early on that, although fungicidal treatment of host trees in the 

forest environment would likely not be practical, treatment of individual high-value 

trees in the urban environment could be feasible and beneficial. Tests (Garbelotto 

and Rizzo 2001, Garbelotto and others 2002c) determined that many of the standard 

chemicals used to control other Phytophthora spp. (Erwin and Ribeiro 1996, Hardy 

and others 2001) were effective against P. ramorum. Metalaxyl, Al-fosetyl, copper 

sulfate, copper hydroxide, and phosphonate were effective against P. ramorum 

in vitro (Garbelotto and Rizzo 2001), and three chemical compounds reduced P. 

ramorum growth rate in potted coast live oak saplings (Garbelotto and others 

2002c). Saplings injected with phosetyl-Al, metalaxyl, and phosphorous acid had 

significantly smaller cankers than untreated saplings or saplings injected with copper sulfate pentahydrate.

Garbelotto and others (2003b) evaluated a variety of commercially available 

chemicals effective against other Phytophthora species on coast live oak (Quercus 

agrifolia Née) and tanoak. Application methods included trunk injections, soil 

drenches, topical applications, and foliar sprays. Treatments with phosphonate 

compounds significantly reduced lesion size in both oaks (Quercus spp.) and 

tanoaks. Injecting the chemicals into the trunk of the tree was the most effective 

method. Treatment of the tree prior to infection was significantly more effective at 

controlling the pathogen than treatment after infection. Phosphonate-treated trees 

remained resistant to new P. ramorum infections for at least 3 months. 

Additional field experiments evaluated the effectiveness of phosphonate chemical treatments for control of P. ramorum in tanoak and Shreve oak (Q. parvula

Greene var. shrevei (C.H. Mull.) Nixon) (Schmidt and others 2006). Native stands 

of mature, uninfected trees were treated with Agrifos® systemic fungicide and 

subsequently inoculated with P. ramorum. Injections as well as topical applications 

of Agrifos with PentrabarkTM (Agrichem, Medina, Ohio) surfactant were evaluated. 

The injection and topical phosphonate treatments significantly reduced lesion size 
87

Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

in tanoaks and Shreve oaks compared to untreated control trees. A combined treatment of injection and topical application methods was most effective in Shreve oak. 

Gabelotto and others (2007) developed and tested bark application of a range of 

phosphite fungicides in combination with the organosilicate surfactant Pentrabark 

on coast live oak. Soil drenches and bark application of all phosphites without surfactant were ineffective. On the other hand, preventive injections of all phosphites 

and bark applications of phosphites amended with Pentrabark were consistently 

effective in suppressing bark colonization by P. ramorum without causing phytotoxicity. 

Kanaskie and others (2006a) compared the efficacy of phosphonate (Agrifos) 

injected into the sapwood with application in combination with Pentrabark surfactant to the trunks of tanoak trees on P. ramorum lesion development. Lesion size 

was significantly smaller in the injected trees than in the bark-spray application 

or control trees. Also, the European isolate caused larger lesions than the North 

American isolate.

Phosphonate (Agrifos) treatments were effective in slowing both infection and 

growth rates for at least 18 months (Garbelotto and Schmidt 2009). Conversely, an 

alternative method consisting of an azomite soil amendment and bark lime wash 

(a previously untested, and unregistered, treatment) was ineffective, and did not 

reduce either growth or infection rates.

Agrifos is registered for oaks in California and Oregon. In California, Agrifos 

is currently recommended as a preventive treatment for use on high-value trees 

and on trees around high-use facilities. Preventive treatment, before infection 

has occurred, is more effective than curative treatments. Trees with advanced 

symptoms of P. ramorum infection (such as multiple bleeding areas, extensive 

beetle attack, evidence of decay, or a sparse or brown canopy) will not benefit from 

treatment. Two application methods are available, injection under the bark directly 

into the sapwood and topical application of the product, mixed with PentraBark 

penetrating surfactant, onto the trunk of the tree. Both methods are effective 

at controlling the growth of P. ramorum in oaks and tanoaks. The phosphite is 

translocated systemically and broken down into phosphonic acid, which triggers 

a defense response in the plant. The host response prevents infection and slows 

down the growth of cankers. Applications should be made when the tree is actively 

transpiring. Avoid treating trees during very hot or very cold weather, or when new 

leaves are emerging. Currently in northern California, two applications in the first 

year are recommended, one fall treatment in November or December and a second 

treatment approximately 6 months later. Subsequent treatments should be made 

once every year, preferably in the fall, alternating between injection and topical 
88

GENERAL TECHNICAL REPORT PSW-GTR-234

application methods. Information on tree treatment, including current recommendations, is summarized at http://nature.berkeley.edu/garbelotto/english/treatment.php.

Treatment of oaks and tanoak, foliar applications—

In early studies, foliar treatment of oaks and tanoaks using phosphonates only provided short-lived protection and caused phytotoxicity (Garbelotto 2004). On coast 

live oak, foliar application of phosphonates amended with surfactants was effective 

only at times and always caused phytotoxicity (Garbelotto and others 2007). The 

practicality and efficacy of aerial application of Agrifos for control P. ramorum in 

Oregon tanoak forests is being tested (Kanaskie and others 2010b). Preliminary 

results indicate small but significant reductions in growth of P. ramorum in Agrifossprayed trees, comparable to the results obtained from bole injection.

Treatment of foliar hosts—

Numerous chemicals to protect foliar hosts from P. ramorum infection have been 

tested. In most cases, fungicides known to be effective against other species of Phytophthora were evaluated. The literature on these studies is summarized in table 5.

Treatment of water and soil—

Treatment of recycled irrigation water with surfactants (Yakabe and Macdonald 

2005), or with mefenoxam and Agrifos (Stringfellow and Reddy 2005), has 

eliminated P. ramorum. Hydrogen peroxide (Jet 5) and sodium hypochlorite (10 

percent) effectively (at label recommended rates) decontaminated water inoculated 

with P. ramorum sporangia (Sansford and Woodhall 2007). In laboratory trials, 

two algaecides with copper-based active ingredients (copper carbonate [Captain®]; 

copper-triethanolamine and copper hydroxide [K-Tea®]) were toxic to zoospores, 

sporangia, and chlamydospores of P. ramorum and to zoospores of six other species 

of Phytophthora (Colburn and Jeffers 2010).

Yakabe and MacDonald (2008) tested chemicals (chloropicrin, 1,3-dichloropropene, dichloropropene with chloropicrin, metam sodium, iodomethane, dazomet, 

dimethyldisulphite, peroxyacetic acid with hydrogen dioxide and zerotol) in artificially infested soil in jars to determine their effectiveness as potential soil treatments. After 2 weeks or the “label minimum re-entry period” (harvest interval), P. 

ramorum was not detected in soils treated with chloropicrin, dichloropropene with 

chloropicrin, metam sodium, iodomethane, or dazomet. The remaining chemicals 

reduced the number of viable propagules, but did not eliminate the pathogen. 

Dazomet (158.8 kg/ 0.4 ha or 350 lb/acre) incorporated throughout the soil profile at 

three ornamental nurseries with infested sites in California eliminated the pathogen 

from treated areas (Yakabe and MacDonald 2008). Metalaxyl-M, added as a soil 

drench to sterile compost inoculated with P. ramorum sporangia, eliminated the 

pathogen (Turner and others 2006).
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Table 5—Fungicides tested on foliar hosts of Phytophthora ramorum for prevention of infection Citation Fungicide P. ramorum host Efficacy/comments

Becker and others Subdue Maxx

®, Aliette

® Rhododendron All were effective foliar treatments for the 

 2010 protection of healthy rhododendrons.Chastagner and Mefenoxam Douglas-fir (Pseudotsuga Pre-bud-break drench completely prevented Hansen 2003; (Subdue MAXX

®) menziesii var. menziesii) infection. 

 Chastagner and Dithane

®, Gavel

®

, Douglas-fir Post-bud-break spray applications provided 100

 others 2005, 2006a Maneb

®, and Polyram

® percent control. 

Champ Formula 2F

®

, Douglas-fir Post-bud-break spray applications reduced

 Reason

®, Daconil infection by 70 to 100 percent.

 Ultrex

®, Stature

®

, 

 and IKF – 916

®

Latron CS-7

® Douglas-fir Post-bud-break spray applications reduced 

 infection by 67 to 100 percent.

PhostrolTM Douglas-fir Post-bud-break spray applications reduced

 infection by 71 to 75 percent.

Silwet L-77

® Douglas-fir Post-bud-break spray applications had no effect 

 on infection.

Chastagner and others Mancozeb (Dithane Noble fir (Abies procera), Foliar application to seedlings protected foliage 2008a 75 DF

®), mancozeb + grand fir (A. grandis) from infection by an EU1 A1 or NA1 A2 isolate.

 zoxamide (Gavel 75 DF

®), dimethomorph 

 (Stature DM

®), cyazofamid

 (Ranman

®), maneb (Maneb

 75 DF

®), metiram 

 (Polyram 80 DF

®), 

 fenamidone (Fenstar

®),

 chlorothalonil (Daconil

 Ultrex

®), potassium 

 phosphite (V-10161

®), 

 pyraclostrobin (Insignia  20W

®), and mefenoxam

 (Subdue MAXX

®)
90

GENERAL TECHNICAL REPORT PSW-GTR-234Chastagner and others Maneb

®, mancozeb + Rhododendron x Effective treatments in controlling disease 

 2008a zoxamide, mefenoxam, “Nova Zembla” development on both wounded and nonwounded

 cyazafamid, dimetho- Rhododendron leaves. morph and mancozeb

Garbelotto and Rizzo Phosetyl-Al, metalaxyl, Coast live oak Injection of potted saplings resulted in significantly

 2001, Garbelotto and phosphorous acid (Quercus agrifolia) smaller cankers than untreated saplings or sap- others 2002c lings injected with copper sulfate pentahydrate.Goheen and others Dimethomorph (Stature

®) Rhododendron macro- Neither fungicide provided complete protection

 2006b and phosphonate phyllum, Vaccinium following foliar application.

 (Agrifos

®) ovatum, California bay 

 laurel (Umbellaria

californica), tanoak

 (Lithocarpus

densiflorus)

Harnik and Garbelotto Metalaxyl (Subdue

®), In vitro All three chemicals were effective in inhibiting

 2006 phosphorus acid hyphal growth, sporangia production, and

 (Agrifos400

®), copper zoospore germination. 

 hydroxide (Champ

®)

Harnik and Garbelotto Copper hydroxide (Champ

®) California bay laurel Foliar application prevented infection up to 6 weeks

 2006 after treatment.

Table 5—Fungicides tested on foliar hosts of Phytophthora ramorum for prevention of infection (continued)Citation Fungicide P. ramorum host Efficacy/comments
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Heungens and others Metalaxyl, dimethomorf, Rhododendron Metalaxyl, dimethomorf, and cyazofamid resulted 2006 cyazofanid, fosphetal Al, in near-complete avoidance of stem infections;

 cymoxanil and mancozeb fosetyl-Al and cymoxanil had intermediate 

 effects; mancozeb was the least effective. Protective effects best when lower leaf surface

 treated day before zoospore inoculation.

Linderman and Menfenoxam (Subdue Rhododendron (cv Drench and foliar applications were effective. Inocu- Davis 2006a Maxx

®), SA 110201 Nova Zembla) lating detached leaves was comparable to inoculat-

 (Sipcam Agro USA, Inc.) ing intact plants to evaluate chemical and biological

 agents against Phytophthora species.

Orlikowski 2004b Phosetyl Al, furalaxyl, Rhododendron All six fungicides significantly inhibited the

 fenamidone + phosetyl pathogen and development of twig blight in lab

 Al, propamocarb + and glasshouse trials, with furalaxyl the most  phosetyl Al, oxadixyl + effective. 

 mancozeb, cymoxanil +

 famoxate

Tjosvold and others Mefenoxam (Subdue Rhododendron Foliar application provided preventive control; 2006a Maxx

®), dimethomorph “Cunningham’s White” post-infection treatments were not effective.

 (Stature DM

®), and R. “Irish Lace” 

 pyraclostrobin (Insignia

®),

 fenamidone

Table 5—Fungicides tested on foliar hosts of Phytophthora ramorum for prevention of infection (continued)Citation Fungicide P. ramorum host Efficacy/comments
92

GENERAL TECHNICAL REPORT PSW-GTR-234 Turner and others Metalaxyl-M (SL 567A), Rhododendron, Viburnum Foliar application of metalaxyl-M, azoxystrobin 2006 dimethomorph/mancozeb and fenamidone/mancozeb on Rhododendron (Invader

®), cymoxanil/ completely inhibited symptom development 

 mancozeb (Curzate M68

®), when applied as protectants either 4 or 7 days

 fenamidone/ mancozeb prior to inoculation. On Viburnum, only (Sonata

®), etridiazole metalaxyl-M was completely effective at all

 (Standon Etridiazole 35

®), protectant timings. Fenamidone/mancozeb was

 azoxystrobin (Amistar

®) effective when applied 4 days prior to inocula-

 and famoxadone/ tion, but not when applied 3 days earlier. cymoxanil (Tanos

®) Fungicides were generally less effective when 

 applied as eradicants. The most effective was metalaxyl-M, completely inhibiting disease

 development when applied 4 days after

 inoculation. None of the fungicides completely  controlled disease development on Viburnum when applied after the same period. 

Wagner and others Dimethomorph (Acrobat

®), In vitro Dimethomorph, copper-octanoate, and mancozeb + 

 2008 copper-octanoate fenamidone inhibited mycelium growth and

 (Cueva

®), and mancozeb zoospore germination. Mancozeb alone did not

 + fenamidone (Gemini

®), inhibit mycelial growth effectively. 

 Mancozeb alone (Dithane Propineb, azoxystrobin, propamacarb, and

 Ultra

® WP), Propineb cyazofamid had no effect on mycelial growth and

 (Antracol

® WG), zoospore germination. 

 azoxystrobin (Ortiva

®),

 propamacarb (Previcur  N

®), and cyazofamid 

 (Ranman

®) 

Table 5—Fungicides tested on foliar hosts of Phytophthora ramorum for prevention of infection (continued)Citation Fungicide P. ramorum host Efficacy/comments
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Pathogen resistance to metalaxyl-M—

Development of resistance to systemic fungicides has occurred with other Phytophthora spp. and is a concern with P. ramorum. Some P. ramorum isolates obtained 

from ornamental nursery plants in the United Kingdom have shown resistance to 

metalaxyl-M (Turner and others 2008b). In Belgium, Heungens and others (2006) 

identified a strain of P. ramorum with decreased sensitivity to metalaxyl-M. Resistance for five European isolates to metalaxyl-M has been reported (Wagner and 

others 2006, 2008). The isolates all originated from nurseries. Alternating the use 

of metalaxyl-M with a different fungicide is recommended to reduce the probability 

of resistance development.

Masking of symptoms by systemic fungicides—

The use of fungicides to control P. ramorum has raised concerns that fungicide 

residues may affect the ability to isolate the pathogen from infected tissue or mask 

symptom development, making it difficult to detect infected plants during routine 

visual inspections. Shishkoff (2005) investigated whether fosetyl-aluminium, 

mefonoxam, or propamocarb hydrochloride have a masking effect on infected 

Rhododendron shoots. The pathogen was recovered following inoculation from 

control and from fosetyl-Al- and propanocarb-treated lesions at high frequencies 

(64 to 100 percent) immediately after treatment, with recovery of the pathogen 

declining thereafter. The pathogen could not be recovered from mefonoxam-treated 

lesions until 3 to 5 weeks after treatment, when low frequencies (3 to 13 percent) 

were found. In all of the treatments, symptoms were not suppressed; lesions 

were easily visible. The pathogen was easily recovered from stem tissue 3 to 5 

weeks after treatment, and sometimes isolated from buds, fallen leaves, and roots. 

Turner and others (2006) reported that P. ramorum could not be recovered from 

Rhododendron and Viburnum leaves 10 days after protectant and eradicant applications of metalaxyl-M, metalaxyl-M with fluazinam, metalaxyl-M with mancozeb, 

metalaxyl-M with chlorothalanil, and propamocarb hydrochloride with fenamidone. 

Results indicated that the chemicals had killed the pathogen and was not merely 

fungistatic. However, Chastagner and others (2010) occasionally isolated P. ramorum from asymptomatic rhododendron tissue inoculated and then treated with 

Subdue MAXX® and Insignia®, suggesting that those fungicides may pose a high 

risk of masking symptom development.

Effects of tree essential oils on the pathogen—

Manter and others (2006) reported that 140 mg/kg of essential oil from the wood of 

Alaska yellow-cedar (Chamaecyparis nootkatensis (D. Don) Spach), Port-Orfordcedar (C. lawsoniana (A. Murr.) Parl.), incense-cedar (Calocedrus decurrens
94

GENERAL TECHNICAL REPORT PSW-GTR-234

(Torr.) Florin), or western juniper (Juniperus occidentalis Hook.) strongly inhibited 

zoospore germination and hyphal growth of P. ramorum in culture. Field tests 

(Manter and others 2008) suggested that heartwood chips from western redcedar 

(Thuja plicata Donn ex D. Don), incense-cedar, and yellow-cedar placed over forest 

litter reduced inoculum potential of the pathogen, and thus, potential for spread. 

Biological

Biological agents are also being tested as protectants. The surfactant-producing 

bacterium Pseudomonas fluorescens strain SS101, known to cause zoospore lysing, 

resulted in significantly less infection of detached California bay laurel leaves by P. 

ramorum (Cohen and others 2006), but results were highly variable. 

Linderman and Davis (2006a) found that bacterial antagonists (Bacillus brevis

and Paenibacillus polymyxa) significantly inhibited all Phytophthora species tested 

in vitro, but were ineffective in inoculation assays of leaves dipped in a cell suspension of each antagonist 24 hours prior to inoculation with P. ramorum or other 

Phytophthora species. Elliott and Shamoun (2008) found that the bacteria Streptomyces lydicus strain WYEC 108 (Actinovate®) and Bacillus subtilis (as found 

in Rhapsody® and Sonata®), applied to detached Rhododendron leaves 24 hours 

before wounding and inoculation with P. ramorum, inhibited lesion development. 

Treatment of whole plants with Rhapsody and Actinovate resulted in some degree 

of protection to the leaves against P. ramorum and reduced the number of foliar 

lesions; effects of Sonata were not significantly different than treatment of plants 

with water (Becker and others 2010).

The soil fungus Trichoderma spp. may provide some control of the soil phase 

of P. ramorum. Widmer (2008) reported that several isolates of Trichoderma were 

mycoparasitic to P. ramorum in vitro, attacking the sporangia and chlamydospores. 

Laboratory assays by Elliott and Shamoun (2008) gave similar results.

Natural Plant Products

Caffeic acid added to V8 juice agar inhibited zoospore germination and sporangial 

germination (Widmer 2008). Application of rice bran extract containing derivatives of caffeic acid applied to Rhododendron leaves prior to infection reduced leaf 

necrosis (Widmer 2008). Agar and soil leachate amended with grapefruit extract 

inhibited colony growth and sporulation of P. ramorum (Orlikowski 2004a). Spraying Rhododendron inoculated with P. ramorum with the grapefruit extract inhibited 

the spread of necrosis on stems and leaves. Pre- and post-inoculation spraying of 

Rhododendron with chitosan also suppressed the disease (Orlikowski 2004a).
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Soil Amendments

Klinger and Zingaro (2006) suggested that symptoms associated with dying oaks 

in P. ramorum-infested areas are sometimes the same as those associated with 

an increase in soil acidity (reportedly due to mosses, industrial pollution such 

as acid rain, acid fog, and other factors), and that the soil acidification weakens 

trees and disposes them to attack by secondary organisms. Thus soil amendments 

containing calcium (applied as lime wash) and other ingredients (usually azomite 

as a fertilizer) to offset soil acidification have been recommended as treatment 

for P. ramorum-infected trees. Scientifically valid studies to support the recommendation are lacking. Garbelotto and Schmidt (2009) reported that an azomite 

soil amendment and bark lime wash treatment was not effective in reducing either 

growth or infection rates of P. ramorum. Increased soil acidity in infested areas has 

apparently not been demonstrated. The addition of calcium does have numerous 

effects on trees and on Phytophthora in vitro and in vivo, both positive and negative 

(Balci and Halmschlager 2003, Campanella and others 2002, Kim and others 1997, 

Messenger and others 2000, Simpfendorfer and Harden 2000, Von Broembsen and 

Deacon 1997). Treatment of potted coast live oak trees inoculated with P. ramorum

with azomite soil amendment and bark lime wash had no effect on bark lesion size 

or infection rates compared to controls (Garbelotto and Schmidt 2009). 

Aluminum-amended peatmoss suppressed chlamydospore production and 

reduced populations of P. ramorum in laboratory trials (Fichtner and others 2008c).

Compost Teas

The use of a liquid tea made from compost to protect hosts of P. ramorum is gaining support among some organic growers and home gardeners. Compost tea, made 

by steeping compost in water with other natural ingredients for at least 24 hours, 

increases the growth of microbes, which may inhibit harmful organisms. The tea 

is sprayed on leaves or used as a soil drench, depending on the part of the plant to 

be protected. The theory is that microbial compounds in the tea destroy harmful 

microbes that attempt to invade plants. Experimental evidence of efficacy in treating P. ramorum hosts is lacking. Linderman and Davis (2006c) treated rhododendron leaves with Paenibacillus polymyxa taken from compost, and then exposed the 

plant to P. ramorum. The P. polymyxa did not protect the plant from damage.

Resistance

A program to develop trees genetically resistant to a pathogen is long term and 

expensive, and has been undertaken in North America for only a few pathogens 

(Sniezko 2006). One successful example of a resistance breeding program for a 
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Phytophthora species is the P. lateralis program for Port-Orford-cedar. A genetics 

white paper developed by the COMTF (Dodd and others 2006) points out the commitment and resources needed to develop a tree resistance program.

Information on the variation in virulence/aggressiveness of P. ramorum and the 

types of genetic resistance in the various host species is limited. 

Resistance in California Bay Laurel and Coast Live Oak 

Studies (Dodd and others 2005, 2008; Garbelotto and others 2003a, Hüberli and 

others 2002) indicated that individuals of California bay laurel and coast live oak 

display differential levels of resistance to P. ramorum. Hüberli and others (2002) 

found a range of resistance, as measured by leaf lesions formed on California bay 

laurel leaves collected from throughout the geographic range of the pathogen, 

following inoculation with P. ramorum zoospores. Dodd and others (2005) found 

significant heritable variation in lesion size on branch cuttings of coast live oak in 

response to inoculation with P. ramorum, and suggested that the variability was 

controlled by several gene loci. Beals and Dodd (2006) found a fairly uniform 

genetic structure in coast live oak throughout its range, with 96 percent of the 

molecular variance occurring within populations. Results suggest that searches for 

Phytophthora-resistant genotypes could be limited to smaller areas of the species’ 

distribution.

The susceptibility of California bay laurel varies geographically. Meshriy and 

others (2006) reported differences in susceptibility to P. ramorum among populations of U. californica, with trees from Oregon being less susceptible, as exhibited 

by smaller lesions following zoospore inoculation of detached leaves, than those 

from California. They found only slight variation among populations from California. The genotypes of the two California bay laurel populations appear to differ, 

and there are physiological differences in the leaf surfaces of California bay laurel 

and Oregon myrtlewood (the common name used in Oregon for U. californica). The 

thicker cuticles of Oregon myrtlewood may reduce the potential for leaf infection.

Based on data from lab susceptibility trials and field infection data collected 

from 97 trees from 12 populations in northern California, Anacker and others 

(2008) found that experimental lesion size and field infection levels differed significantly among both California bay laurel trees and populations. The phenotypic trait 

of leaf area was significantly related to lab lesion size, where bigger leaves produced 

bigger lesions. Variability in lesion size produced in the lab and infection levels 

in the field were significantly related to amplified fragment length polymorphism 

(AFLP) markers, suggesting a genetic basis to resistance. They also identified markers associated with phenotypic traits putatively involved in conferring resistance, 

including leaf toughness and leaf water content. 
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Resistance in Tanoak

Hayden and Garbelotto (2006) demonstrated differences in resistance among 

tanoak individuals and populations, suggesting the existence of quantitative resistance to P. ramorum in tanoak populations and individuals. Bark and wounded 

leaf-inoculated tanoak saplings grown from acorns collected in the Six Rivers 

National Forest showed significant variability in lesion size among individuals, with 

stem lesion area positively correlated with leaf lesion area. In their study, growing conditions also had an effect with trees in south-facing rows of the lath house 

having smaller lesions than those in north-facing rows. Additional inoculations of 

seedlings (using detached leaves and seedling tips) from nine sites revealed variable 

resistance with significant heritability (Hayden and others 2010). 

Resistance in Viburnum 

Grünwald and others (2006a) found a considerable range of resistance in the genus 

Viburnum. They evaluated nine species of field-grown Viburnum (23 cultivars) 

for resistance to P. ramorum in detached leaf tests. They obtained significant 

differences between cultivars in percentage of leaf area affected (P < 0.001), with 

no significant differences owing to isolates or interactions between isolates and 

cultivars. The percentage of leaf area affected ranged from 95 percent in extremely 

susceptible cultivars (cvs. V. burkwoodii cv. unkown, V. plicatum var. tomentosum

cv. Mariesii, and V. trilobium cvs. Alfredo and Bailey), to between 25 and 90 percent in a moderately susceptible group (cvs. V. burkwoodii cv. Mohawk, V. lantana

cv. Mohican, V. opulus cvs. Compacta and Hanum, V. lentago cv. unknown, V. 

sargentii cv. Onandaga, V. trilobium cv. Redwing) to less than 15 percent infection 

in the most resistant group (V. dentatum cvs. Autumn Jazz, Blue Muffin, Chicago 

Lustre, and Burgundy; V. opulus cv. Sterile, V. plicatum cvs. Newport, Popcorn, 

Shasta, and Shoshon; V. nudum cv. Winterthur, V. trilobium cv. Wentworth). 

Resistance in Lilac 

Grünwald and others (2006b) evaluated the relative susceptibility of 25 species and 

cultivars of lilac to P. ramorum using detached leaf assays. The cultivars tested had 

significantly different percentage of leaf area affected. Cultivars Syringa vulgaris 

cv. Ellen Willmott, Syringa x prestoniae cv. Minuet, and S. vulgaris cv. Katherine 

Havemeyer had less than 20 percent leaf area affected and were the most resistant.

Resistance in Rhododendron

Tooley and others (2002) found that leaves of Rhododendron “P.J.M.,” R. maximum, 

and R. carolinianum dipped in suspensions of P. ramorum sporangia developed 
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lesions on less than 10 percent of the leaf area compared to a highly susceptible 

cultivar like Cunningham's White that developed up to 50 percent leaf area infected 

with the most virulent isolate tested. 

De Dobbelaere and others (2006) screened 63 Rhododendron species (21 

species and 42 hybrids) for their susceptibility to P. ramorum. Four inoculation 

methods (wounded or nonwounded detached leaves and wounded or nonwounded 

branches) were used. Methods involving nonwounded tissue were used to estimate 

the ability of the hosts to resist tissue penetration. Methods involving wounded 

tissue evaluated the resistance to pathogen growth inside leaf tissue. Significant differences in disease susceptibility were observed between species as well as between 

hybrids with all methods used. Inoculation of wounded leaves and stems showed 

that most species and hybrids were susceptible to some extent. Inoculation of 

nonwounded leaves or stems resulted in more variation in susceptibility, with little 

to no infection occurring in a few hybrids. The results suggested that if significant 

resistance is present, it probably occurs at the level of tissue penetration. 

Linderman and others (2006) tested different species of Phytophthora or 

isolates of P. ramorum (both mating types) by inoculating detached leaves of “Nova 

Zembla” rhododendron, lilac (Syringa vulgaris L.), or doublefile viburnum (Viburnum plicatum Thunb. var. tomentosum). Plant species within genera or cultivars 

within species varied in susceptibility to isolates of P. ramorum and other species 

of Phytophthora. Phytophthora ramorum, P. citricola, P. citrophthora, and P. 

nicotianae were the most virulent pathogens on most of the host plants inoculated. 

Some plants were susceptible to several species of Phytophthora, whereas others 

were susceptible only to P. ramorum.

Resistance in Vaccinium

Parke and others (2002b, 2002c) compared the potential susceptibility of wild Vaccinium species and of commercial Vaccinium crops such as blueberry (Vaccinium

spp.), cranberry (V. macrocarpon Aiton), and lingonberry (V. vitis-idaea L. ssp. 

minus (Lodd.) Hultén) in detached leaf assays. A wide range of disease responses—

from resistant (cranberry) to highly susceptible (lingonberry)—was observed 

among the Vaccinium species and among cultivars. 

Survey and Monitoring

For the disease management strategies discussed here to be implemented correctly and efficaciously, it is essential to know the distribution and incidence of the 

pathogen. Detection efforts are done through surveys and monitoring. Monitoring 

to detect P. ramorum presence is a critical component of the USDA national P.
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ramorum management strategy (USDA APHIS 2005b). The national strategic plan 

strives to prevent artificial spread of P. ramorum through prevention, detection 

and monitoring, and control and management. The objective of the detection and 

monitoring component of the strategy is to rapidly and accurately determine where 

the pathogen and disease are located and to reliably verify pathogen presence or 

absence in areas considered to be uninfested. The plan discusses detection and 

monitoring needs such as port inspections, nursery surveys, aerial and roadside 

surveys in wildland and urban forest settings, forest inventory and monitoring plots, 

and public employees trained to look for the disease.

Aerial and ground-based surveys and image analysis are used in California and 

Oregon forests and woodlands containing host species to determine the distribution 

and incidence of P. ramorum. In addition, research information on hosts, likely 

pathways of pathogen movement, and favorable climatic conditions are being used 

in a risk-based analysis to plan surveys to detect P. ramorum (Goheen 2003). For 

information on remote sensing and other specific image analysis projects, see the 

University of California Web site http://kellylab.berkeley.edu/oakmapper/. The 

USDA FS Western Wildland Environmental Threat Assessment Center has an 

ongoing project to evaluate the use of hyperspectral imagery for previsual detection 

of P. ramorum-infected tanoak trees. Preliminary results suggest that identifying 

infected tanoaks may be possible, but not in situations where the infected trees are 

below the tree canopy (http://gis.fs.fed.us/wwetac/projects/completed/hyperspectral.

html).

Forest Survey and Monitoring in California

California's P. ramorum monitoring program focuses on early detection. Aerial and 

ground-based surveys of uninfested areas within minimally infested counties or 

counties with no known occurrence of P. ramorum but sharing a common border 

with infested counties are conducted, and ground-based early-detection surveys in 

high-risk uninfested areas are done (Mai and others 2006, Mark and Jirka 2002, 

Meentemeyer and others 2006). Early detection efforts include monitoring of 

streams and rivers throughout infested and at-risk areas of California by baiting 

with rhododendron leaves (Aram and Rizzo 2010, Murphy and others 2006). 

Forest Survey and Monitoring in Oregon

Several P. ramorum detection surveys are conducted each year in at-risk forest 

areas by the Oregon Department of Forestry and the USDA Forest Service (USDA 

FS) (Goheen and others 2006a). The forest range of tanoak is systematically 

surveyed from a fixed-wing aerial survey plane, and suspicious trees are mapped. 

Followup helicopter surveys provide a closer look at symptomatic trees and enable 
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more precise mapping. All suspected trees are checked from the ground and 

samples collected for confirmation. In addition, annual ground surveys check the 

perimeters of previously treated areas for newly infected trees. Oregon nurseries, 

Christmas tree plantations, and other sites are surveyed regularly, as mandated by 

federal regulations (Osterbauer and others 2004).

Streams in and near the quarantine area in southwest Oregon are monitored 

for P. ramorum using rhododendron and tanoak leaves. The leaf baits are collected 

and replaced every 2 weeks throughout the year. Collected leaves are assayed by 

multliplex rDNA internal transcribed spacer polymerase chain reaction (ITS PCR). 

Initially, both isolation on a selective medium and ITS PCR were used, but ITS 

PCR was more sensitive. When infected leaves are detected, ground surveys are 

used to locate infected hosts upstream (Sutton and others 2009). 

National Surveys

A national survey of forests at risk is conducted by the USDA FS Forest Health 

Monitoring program and its cooperators to determine whether the pathogen occurs 

outside the quarantined areas of California and Oregon. As a first step, the USDA 

FS produced a risk-based U.S. map identifying sampling polygons. Factors used 

to assign risk and develop the sampling polygons were (a) presence of known host 

species, host genera, and closely related genera; (b) locations of nurseries receiving 

Rhododendron spp. stock; (c) length of yearly mesic/moist weather period; and (d) 

area outside limiting temperature extremes currently associated with P. ramorum. 

Based on these criteria, much of the southern Appalachian and the Pacific coastal 

regions are currently rated high risk. Additional information on the national survey, 

including the methods used and a copy of the national risk map, are available in 

chapter 4.

Both APHIS-PPQ and the states conduct a national survey of nurseries annually through the Cooperative Agricultural Pest Survey program. The USDA FS 

and states conducted nursery perimeter and general forest detection surveys using 

terrestrial vegetation survey protocols from 2003 to 2006. Successful pilot testing 

of stream baiting survey protocols in 11 states during 2006 resulted in full implementation in 2007, and the more cost-effective stream baiting methods and protocols continued to the present (Oak and others 2010). Table 2 in chapter 2 presents 

nationwide nursery detections of P. ramorum by year.

Canadian Surveys

The Canadian Food Inspection Agency (CFIA) conducts annual surveys—targeting 

importing nurseries, botanical and public gardens, and collections of rhododendron 

societies—for P. ramorum. When P. ramorum is found, the nursery site is placed 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

under quarantine and all infected plant material is destroyed. Extensive surveys and 

trace-forward and trace-back activities are then conducted to ensure the organism 

has been eliminated (http://www.inspection.gc.ca/english/plaveg/pestrava/phyram/

sodmsce.shtml). As stated earlier in this chapter, samples originating from 9 retail 

nurseries and 12 landscape sites in British Columbia were positive for P. ramorum

in 2009.

EU Surveys

In the European Union, annual surveys are required and reported by all EU member 

states as part of the European Union emergency measures for P. ramorum (Slawson 

and others 2008). In the United Kingdom, surveys of the natural and seminatural 

environment have included the use of water baiting for detecting the pathogen in 

water-catchment areas (Sansford and others 2009). Detections of the pathogen in 

England and Wales in retail and nursery sites and in established gardens, woods, 

and other natural sites are shown in figs. 15 and 16.

Ongoing outbreaks

Eradicated outbreaks

Figure 15—Detection of Phytophthpra ramorum at retail and nursery sites in England and 

Wales, 2002 to 2009. Source: http://www.fera.defra.gov.uk/plants/plantHealth/pestsDiseases/documents/pRamorumOutbreakMaps.pdf. (June 2010).
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Efforts to model the potential habitat for P. ramorum are also important for 

disease regulation and management. Those modeling efforts are discussed in 

chapter 4.

Additional Management Actions

Rizzo and others (2005) discussed what they considered to be the necessary 

components of a management program for P. ramorum in California and Oregon 

forests. In addition to components that have been summarized here (monitoring, 

eradication, use of fungicides, and prevention of human spread), they add diagnosis, 

restoration, fire, and stand manipulation. Diagnosis is covered in chapter 2; it is a 

key aspect of management, as detection and identification are critical to the success 

of management/control measures. Restoration efforts involving revegetation will be 

Ongoing outbreaks

Eradicated outbreaks

Outbreaks on trees

(lethal bleeding cankers)

Figure 16—Detection of Phytophthora ramorum in gardens, woods, and other natural sites in 

England and Wales, 2002 to 2009. Source: http://www.fera.defra.gov.uk/plants/plantHealth/

pestsDiseases/documents/pRamorumOutbreakMaps.pdf. (June 2010).
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

dependent on results of host resistance studies. Stand manipulation efforts in California and Oregon are discussed earlier in this chapter under “Eradication.” A brief 

summary of research on fire in relation to P. ramorum management follows here.

Fire

Prescribed fire has been used as a tool to restore and maintain natural ecosystems 

and control tree diseases elsewhere (Brennan and Hermann 1994, Harvey 1994). 

Because the first reports of P. ramorum impact in California forests were in urban 

areas with a history of fire suppression, some have suggested that the absence of fire 

may have created stand conditions favoring the pathogen (Moritz and Odin 2005, 

Rizzo and others 2002b). Moritz and Odion (2005) found a strong negative relationship between P. ramorum infections across northern California and the locations of 

fires since 1950. Their data analysis supported the hypothesis that past fire suppression is somehow important in the spread of the disease. However, in a more detailed 

study of Sonoma County only, evidence for a negative relationship between the 

disease and fire history was not as strong (Moritz and Odion 2006), pointing out the 

complex interactions involved among fire, the disease, and its management at the 

landscape level. A relationship between fire suppression and disease incidence does 

not necessarily indicate a causal relationship. 

It is unlikely that prescribed fire would be an effective management option in 

the heavily populated areas of central coastal California. The effects of prescribed 

fire on P. ramorum are being studied in efforts to slow the spread in Sonoma, Mendocino, Humboldt, and Del Norte Counties in north coastal California (Valachovic 

and others 2010a). In southern Humboldt County, a 20.2-ha infested site was treated 

by removal of all tanoak and bay laurel trees. Half the site was subsequently underburned. Site monitoring recovered P. ramorum from spore traps and soil infrequently, and usually in association with heavy densities of bay laurel sprout clumps 

or where residual bay and tanoak trees were missed during treatment (Valachovic 

and others 2008, 2010a). This, together with the Oregon results where P. ramorum

persisted in underburned sites, suggests that burning can be a tool in cleaning up 

small infectious material in infested sites, but that the pathogen may persist at low 

levels. Beh and others (2010) recovered P. ramorum from streams in Big Sur areas 

that had experienced severe wildfire (and no other treatment) the previous season. 

Summary

An attempt was made here to compile and summarize the existing literature 

on management and control of the diseases caused by P. ramorum. The pitfalls 

involved with attempting to summarize the literature associated with an active and 
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evolving area of research such as P. ramorum are many. A synthesis of that 

literature is difficult, as new findings and ongoing projects take time to become 

public or are published. The reader should make use of the various Web sites 

available to obtain the most current information. Useful Web sites on regulations 

and quarantine include an APHIS site http://www.aphis.usda.gov/ for U.S. regulations; the various state regulatory sites such as (http://www.cdfa.ca.gov/phpps/pe/

InteriorExclusion/SuddenOakDeath/), and (http://www.oregon.gov/ODA/PLANT/

NURSERY/reg_sod.shtml); and the U.K. site (http://www.fera.defra.gov.uk/plants/

plantHealth/pestsDiseases/pRamorum.cfm) for international information. Information on recently completed and ongoing studies on eradication, protection, and 

resistance can be found in monthly reports issued by the COMTF at www.

suddenoakdeath.org.

Several recent publications illustrate how control options are being used as part 

of an overall P. ramorum management program. Valachovic and others (2010b) 

summarized some representative available treatments (including both tested and 

untested), for Humboldt County in California where tanoak is the primary host 

(table 6). The treatments were summarized according to the primary P. ramorum

management goal on that property: (1) minimizing property impacts from the 

pathogen; (2) strategic protection of tanoak islands, old-growth tanoak, or particular 

geographic areas; and (3) suppression of P. ramorum and limitation of spread. 

Table 6—Matrix of Phytophthora ramorum management goals and possible treatments

Minimize property Strategic protection of oak/tanoak islands, Suppression of P. ramorum and

impacts old-growth trees, or geographic area limiting spread

Dead tree removal Manual removal of bay laurel only Manual removal of bay laurel and tanoak

 (± prescribed underburning)

Reforestation Agri-fos® application Modified fuel hazard reduction removal

 (± bay girdling)

Maintain some tanoak, Combination of manual removal Herbicide host removal (bay laurel

 with thinning of bay laurel and Agri-fos and tanoak)

 (manually or with application

 Agri-fos)

Source: Valachovic and others 2010b.
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Table 7—Sudden oak death strategic planning efforts at Redwood National and State Parks 

Strategy Goal Action

Current efforts (P. ramorum not present)

Prevention To keep P. ramorum out of Education/outreach, best management practices, 

 RNSP as long as possible information signs, public Web page, sanitation, 

 gravel high-risk areas

Early detection To find the pathogen before it Stream baiting, ground surveys, aerial surveys,

 becomes established in the host modeling

 landscape

Management To develop and implement a Communicate with regulatory agencies, adjacent

 planning sound management strategy to landowners, and interested public on the full array

 combat this disease in the park of options available for managing the disease

 consistent with park values and authority

Future potential efforts after P. ramorum arrives in park

Eradication To eliminate pathogen before it Set quarantine area; some combination of herbicide,

 spreads to uninfested sites cut, burn; monitor treated sites

Protection/ To strengthen important trees Chemical treatments: 

 containment near infection sites and to Agri-fos–tanoaks 

 prevent human and natural Physical treatments:

 transmission of the pathogen Host removal in potential spread areas (buffers)

 Trail closures

 Cleaning stations

Restoration/ To conserve ecologically Plant resistant hosts (if available);

 conservation important oaks and tanoaks in plant conifers and other species

 the landscape, rehabilitate Identify tanoak refuges and protect

 infection sites and minimize through physical and chemical buffers

 ecological impacts

Source: Adapted from Bueno and others 2010.

Redwood National and State Parks in northern California are developing a 

sudden oak death management plan before the disease arrives in the parks (Bueno 

and others 2010). The goal is to slow the arrival of P. ramorum by implementing 

preventive measures; to prepare for its arrival by conducting early detection for 

the pathogen and modeling the potential niche of its most important hosts; and to 

address the actions needed to confront the disease once it arrives. The Redwood 

Parks management plan (Bueno and others 2010) summarizes the actions available 

to manage P. ramorum in California forests (table 7). 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Chapter 6: Economic and Environmental 

Impacts of Phytophthora ramorum

Introduction 

The introduction and establishment of the exotic pathogen Phytophthora ramorum

into native forest ecosystems of California and Oregon; into the nursery/ornamental 

trade of the United States, Canada, and Europe; and into European gardens and 

landscapes have had significant economic and environmental impacts. Establishment of the pathogen in areas such as the hardwood forests of the Eastern United 

States where known susceptible hosts occur will have additional impacts. 

This chapter is not intended to be an economic analysis, but rather summarizes 

the literature on the economic and environmental impacts of P. ramorum. The 

economic impacts section discusses the resources at risk (benefits of hosts/products) 

and the costs of P. ramorum in forests and woodlands, urban forests, and Christmas 

tree plantations; on forest products other than timber and other forest values; in the 

nursery industry; and in the cut flower and foliage industry. The environmental 

impacts section summarizes the literature on the benefits provided by ecosystems 

and the effects of P. ramorum (potential for ecosystem destabilization, reduction in 

biodiversity, reduction or elimination of keystone species, reduction or elimination 

of endangered or threatened species) on recreation and on wildlife.

Economic Impacts

Forests/Woodlands, United States

Resources at risk—

California oak woodlands contain about 5 billion ft3 (142 million m3) of wood 

with a stumpage value over $275 million (Kliejunas 2003). The 5.8 billion ft3

 (164 

million m3) of oaks (Quercus spp.) in nearby California timberlands are worth over 

$500 million for forest products alone (Kliejunas 2003). Oak products exported 

from California from 1996 through 2000 averaged almost $50 million per year 

(USITC 2005). In the United States as a whole, the export market value of red oak 

logs and lumber in 2002 was over $300 million (USITC 2005). 

In Oregon, the annual timber harvest value (mostly Douglas-fir [Pseudotsuga 

menziesii (Mirb.) Franco]) of the four southwest Oregon counties (Josephine, Coos, 

Curry, and Douglas) where tanoak (Lithocarpus densiflorus (Hook. & Arn.) occurs, 

based on 2006 data, is $1.68 billion per year (Kanaskie and others 2008b). Although 

neither tanoak nor coast live oak (Quercus agrifolia Née) is a commercial timber 

tree in California or Oregon, tanoak is harvested in Oregon for the chip market 

when prices warrant. 
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Costs—

The major impact of P. ramorum in forests of the United States has occurred in 

the mixed-evergreen and redwood-tanoak forests of coastal central California. 

Although damage on coast redwood (Sequoia sempervirens (Lamb. ex D. Don) 

Endl.) and Douglas-fir from P. ramorum is limited to foliage and small branches, 

regulatory actions to prevent spread of the pathogen (for example, requiring 

removal of small branches, washing soil from logs) could impact (presumably in 

the form of lost markets) the redwood and Douglas-fir industry in California at an 

estimated $50 million a year (USDA 2005). As an example, 2009 was the first year 

in over 20 years with an abundant redwood cone crop. Seed collection costs were 

increased by the need to comply with P. ramorum regulations that prohibit movement of redwood twigs and needles out of the infested coastal California counties. 

Every cone had to be clipped by hand, costing an estimated $100 per bushel for 

the 300 bushels collected (Frankel 2009). Any regulations imposed to limit spread 

may also affect timber harvest and trade in the commercial Douglas-fir forests in 

Oregon, Washington, and western Canada.

In Oregon, potential losses of at least $100 million per year in stumpage value 

(lost harvest) are estimated if eradication is not successful and P. ramorum spreads 

uncontrolled in southwest Oregon (Kanaskie and others 2008b). Between 2001 and 

the end of 2008, eradication treatments in Curry County, Oregon, were completed 

on approximately 2,400 ac (971 ha) of forest at a cost of $4.3 million (Kanaskie 

and others 2008a, 2008b). Additional costs to monitor and manage the eradication 

program (environmental documentation for treatment, for example) have been 

incurred.

An economic analysis was performed including three control scenarios in 

Oregon forests—continue the current control program (removal and destruction of 

all host plants within a 100-m radius when current monitoring discovers an infected 

plant), increase the control program in an attempt to eradicate the pathogen from 

Oregon forests within 5 years (increase the level of monitoring and control), and no 

control program (monitoring only) (Hall and Albers 2009). The analysis assumed 

that each policy would affect costs by altering the rate of spread of the pathogen 

and thus determine the rate of increase in the quarantine area. Costs to agencies as 

a result of program implementation and costs to the forest products industry as a 

result of P. ramorum quarantine regulation were projected out for 20 years under 

the three scenarios. A variety of other costs were not included (a reduction 

in Oregon’s forest product export market, a reduction in the nontimber forest 

product market, and increased production costs for producers utilizing P. ramorum

host plants). The estimated costs and benefits associated with each program are 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

summarized in table 8. The wide range in benefit estimates (from negative $9 

million to positive $1.2 billion) results from basing the estimates largely on the 

uncertain spread rate of P. ramorum in Oregon forests.

The economic value of Eastern U.S. timber species would be significantly 

reduced if P. ramorum were to become established there. Two oak species (Quercus 

rubra L. and Q. falcata Michx.) native to the Eastern United States were found 

naturally infected in Europe (Brasier and others 2004a), and susceptibility of other 

Eastern U.S. tree species (Q. alba L., Q. laurifolia Michx., Q. nigra L., Q. pagoda

Raf., Q. phellos L., Q. prinus L., Q. virginiana Mill., Acer saccharum Marsh., 

Juglans nigra L.) has been experimentally demonstrated (Brasier and others 2002, 

Linderman and others 2007, Tooley and Kyde 2007). The potential economic threat 

from the pathogen to commercial timber production from oak hardwood forests in 

the United States has been estimated as exceeding $30 billion (Kliejunas 2003). 

The pathogen has affected international trade. Numerous countries have placed 

restrictions on the movement of affected plants and plant parts from the United 

States (Rizzo and Garbelotto 2003), thus reducing potential markets for forest hosts 

of P. ramorum. Worldwide, the European Union pest risk analysis for P. ramorum

(Sansford and others 2009: appendix 4) lists 68 countries for which P. ramorum is 

either on their lists of regulated pests or mentioned in their legislation.

Forests/Woodlands, Canada and Europe

To date, no tree species have become affected in woodlands or forests in Canada, 

and no timber plantations have become affected in the European Union. Because 

widespread mortality in forests in Canada, the United Kingdom, and the European 

Union has not occurred, potential economic losses owing to P. ramorum have not 

been quantitatively estimated. The estimated annual value of timber in the United 

Kingdom is (in 2003 figures) about £36 million (Sansford and Woodhall 2007). 

Kehlenbeck (2008) estimated that in the “Northern European Tree Host System” 

(broadly defined as trees with stem cankers in association with infected rhododendron in the Netherlands and the United Kingdom) present impacts are moderate 

and restricted to few areas where Rhododendron are associated with tree hosts and 

Table 8—Estimated costs and benefits associated with control 

programs in Oregon forests

Control program Cost Benefit

Million dollars

None 21.3 to 1,238.5 0

Current 27.5 to 33.4 -6.2 to 1,205.1

Eradication 30.4 to 31.5 -9.1 to 1,207.0
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GENERAL TECHNICAL REPORT PSW-GTR-234

environmental impact is caused. Kehlenbeck (2008) estimated the potential impact 

to be not more than moderate where no widely distributed foliar hosts of Northern 

European forests occur. In the “Southern European Tree Host System,” present 

impacts are minimal, but potential impact is predicted to be major if P. ramorum

were introduced and spread in the unique Mediterranean laurel and Q. ilex L. 

forests (Sansford and others 2009). 

If P. ramorum were to become established in timber plantations in the European Union, there is a potential risk of tree death of a range of species including 

beech (Fagus sylvatica L.) and oak (Quercus spp.), as trees of these species have 

died from the pathogen in the United Kingdom and the Netherlands. Based on 

climatic conditions most similar to California and Oregon, the areas most likely to 

become affected are northwest Spain, northern Portugal, southwest England, and 

parts of Italy and western Albania. The long-term impact was estimated to be minor 

to moderate in the absence of controls (Sansford and others 2009).

The United Kingdom has provided £25 million for a 5-year program (2009 to 

2014) to contain and eradicate P. ramorum and P. kernoviae in historical gardens, 

woodlands, heathlands, and from nurseries and retailers in England and Wales. 

As part of that program, a control strategy for P. ramorum will include removal of 

the sporulating host Rhododendron ponticum L. from woodlands, heathlands, and 

public gardens. Based on work in Cornwall, United Kingdom, the costs of clearance for R. ponticum (as a control strategy for both P. ramorum and P. kernoviae) 

are estimated at £7,000 per ha for woodland and £10,000 per ha for public gardens 

(Sansford and others 2009). However, in some situations removal is seen as a 

benefit, as it would lead to an increase in biodiversity of woodlands and heathlands. 

Sansford and others (2009) presented an analysis indicating that the biodiversity 

benefits from undertaking clearance of understory R. ponticum for disease control 

is £3 million over 20 years. Removal of R. ponticum from heathlands is also seen as 

a benefit because biodiversity and heathland condition would improve. Sansford and 

others (2009) calculated a benefit (as a reduction in heathland loss) of £20,000 over 

20 years.

Urban Forests 

Resources at risk—

In coastal central California, the value of oak woodland suitable for residential 

development has been estimated at $20,000 per ac (0.4 ha); rangeland with at least 

40 oaks per ac (0.4 ha) was worth 27 percent more than open land (Standiford 

2000). In southwestern Oregon, mature black oak trees can increase property values 

by $5,000 to $30,000 (Osterbauer 2003). 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Costs—

Kovacs and others (unpublished data1) found a decrease in property values in the 

north Bay Area (Marin County) of California with proximity to areas affected by

P. ramorum (proximity to oak woodlands, confirmed infections, aerial-observed 

oak mortality, or arborist-reported oak mortality). They found a 2 to 5 percent lower 

value for properties within a quarter mile of oak woodlands infested with P. ramorum, and a 5 to 8 percent lower value for properties with confirmed infected trees; 

the property value rebounds when infected trees are removed.

Tree mortality resulting from P. ramorum increases risk from tree failure and 

more intensive fires because of increased fuel loads from dead trees. In California, 

landowners in the infested areas have to pay for the costly removal of dead trees to 

protect homes and property. Kovacs and others (see footnote 1) estimated a removal 

and treatment cost of $20.5 million over a 10-year period (1998 to 2007) in urban 

areas of Marin County, California. A survey of arborists in Marin County, California, found that the average cost of oak tree removal was $1,700 per tree; average 

cost of pruning or removal of California bay trees was $600 (see footnote 1). In 

Oregon, the cost for removal of a single dead tree from a homeowner’s property 

was as high as $3,000 (Osterbauer 2003). Economic losses from removal of infected 

Quercus trees may be partially offset by utilization of the material for wood products (Shelly and others 1996). 

Two small (less than 1 ha) fires (one in Napa County and one in Sonoma 

County) have been caused by dead trees (P. ramorum-infected) snapping and 

hitting power lines (Frankel 2008). Power company cost of dead tree removal to 

prevent power line damage is extremely variable depending on accessibility, tree 

size, and other factors. Estimates in the Big Sur region of coastal central California 

begin at about $600 per tree. During a 3-year period (April 2002 through March 

2005), the state of California spent $1.5 million on hazard tree removal in five P. 

ramorum-infested counties (Marin, Sonoma, Alameda, Santa Cruz, and Monterey). 

Additional costs of the hazard tree program included $205,000 for hazard tree 

assessment and about $71,000 for restoration (Jones 2009). In 2009, the Santa Clara 

Fire Safe Council received a $150,000 grant for removal of hazard trees resulting 

from P. ramorum-caused mortality (Frankel 2009).

Preventive treatments of oaks in urban areas with the systemic fungicide 

Agri-fos® are expensive as well as potentially harmful to the environment if used 

incorrectly. A limited survey of arborists in Marin County, California, found 1,400 

customers with treatments in the seven companies surveyed, at an average cost of 

1 K. Kovacs and J. Englin, University of Nevada, Reno; T. Holmes, USDA FS, Southern 

Research Station, Research Triangle Park; J. Alexander, UC Cooperative Extension, Marin 

County.
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GENERAL TECHNICAL REPORT PSW-GTR-234

$115 per treatment (see footnote 1). The current recommendation is for reapplication 

each year, so these costs to homeowners (but benefits to arborist companies) may 

accumulate over time.

A strategic plan for Sonoma County, California (Bell and others 2008), summarizes needed funds for an effective P. ramorum management program in the first 

and subsequent years (table 9). Estimated costs are for hazardous tree management, 

practices to slow the spread, education of agencies and publics, and fuels reduction 

in the urban/wildland interface. 

Christmas Tree Plantations

Resources at risk—

Nationwide, the Christmas tree industry had a wholesale value of $520 million in 

2003 (Cave and others 2008, Jerado 2004). Of that value, Oregon produced $158 

million, Washington $60 million, and California $10.4 million (Jerado 2004, USDA 

2005). 

Costs—

Expansion of establishment of P. ramorum in the industry and resulting regulation 

on trade would likely have significant, but unknown, economic impact. A major 

Christmas tree species, Douglas-fir, is a host of P. ramorum. Other Christmas tree 

species have been found naturally infected (grand fir [Abies grandis (Douglas ex 

D. Don) Lindl.], white fir [A. concolor (Gord. & Glend.) Lindl. ex Hildebr.], red fir 

[A. magnifica A. Murr.]) or susceptible in laboratory trials (Chastagner and others 2006b). The pathogen has been detected in Christmas tree plantations in the 

Table 9—Summary of needs and costs, Phytophthora ramorum 

management in Sonoma County, California

Estimated costs 

Anticipated needs Year 1 Subsequent years

Thousand dollars

Fire fuels reduction/mitigation 2,000.0 2,060.0

Tree removal and treatment/forest health 867.1 639.1

Education and outreach 313.1 296.1

Develop fuel model 200.0 0

Hazardous and infected tree survey 614.2 122.6

Staff training 36.5 37.6

Develop sudden oak death protocols 30.0 0

Fire fuels survey and mitigation plan 30.0 0

Fire department funds 16.2 162

 Total 4,107.1 3,171.6
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

infested area of California, but primarily only in the vicinity of infected California 

bay laurel (Umbellularia californica (Hook. & Arn.) Nutt.) or other sporulating 

hosts (Chastagner and others 2008d). In one instance, Chastagner and others 

(2008b) found infection of a few white fir and Douglas-fir Christmas trees under a 

black walnut (Juglans nigra L.) tree that was infected with mistletoe (Phoradendron

serotinum subsp. macrophyllum); the mistletoe was a host of P. ramorum. However, 

their data and the inability of P. ramorum to spread from conifer to conifer suggest 

that there is a very low risk of P. ramorum developing in Christmas tree plantations that are not associated with infected high-inoculum producing plants, such 

as California bay laurel. Regulating small branches and twigs of affected species 

essentially limits movement of host Christmas trees out of regulated areas.

Forest Products Other Than Timber

Resources at risk—

Products crafted from native materials in coastal California, Oregon, and Washington forests are economically significant. High-value uses for hardwood hosts of P. 

ramorum include custom furniture, flooring, cooperage, and tool handles (Shelly 

and others 1996). Other uses for wood from hardwood hosts include firewood, 

wood chips for pulping, mulch, compost, nongrade lumber, and charcoal (Cave and 

others 2008). In 2000, the Chetco Ranger District on the Rogue River-Siskiyou 

National Forest in Oregon sold permits for 51 900 kg of tanoak boughs, 8400 kg 

of huckleberry (Vaccinium spp.) foliage, 5000 kg of madrone (Arbutus menziesii

Pursh) boughs, 100 huckleberry transplants, and about 49 900 kg of miscellaneous 

boughs and foliage (Zepeda 2001). The foliage of evergreen huckleberry (Vaccinium

ovatum Pursh), used as browse by elk, is harvested for use in floral arrangements. 

In the 1970s, an estimated $1 million worth of foliage was harvested annually in 

western Washington (Minore 1972). Huckleberries are an important secondary forest product from Pacific Northwest forests. Volume harvested varies. The wholesale 

price of huckleberries (includes species in addition to V. ovatum) ranged from $2.98 

to $2.19 per lb (0.45 kg) in 1995 and 1996 (Osterbauer 2003).

Costs—

The economic impacts of P. ramorum on forest products other than timber have not 

been estimated.

Other Forest Values

Other benefits of forests, such as water and watershed protection, grazing, wildlife 

food and habitat, and recreation (Thomas 1997) are usually considered environmental benefits rather than economic, and are discussed in that section.
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GENERAL TECHNICAL REPORT PSW-GTR-234

Nursery Industry, United States

Resources at risk—

In 2006, the U.S. domestic production of nursery crops was valued at about $12.9 

billion. Imports for these crops were $341 million and exports were $287 million 

(Jerado 2007, as cited in Cave and others 2008). The U.S. ornamental nursery 

industry is valued at over $13 billion annually, ranking as the third-highest-value 

crop in the United States. California is the industry’s leading producer of horticultural plants, valued at $2 billion a year. Oregon’s industry is ranked fifth nationally 

and ranks second in the production of woody plants (USDA 2005). In 2006, the 

wholesale value of nursery stock sold in Oregon was $966 million (USDA NASS 

2007).

Costs—

The U.S. nursery industry has been strongly affected by P. ramorum. Surveys in 

March 2004 detected P. ramorum in two large southern California nurseries that 

had shipped potentially infected plants to over 1,200 nurseries in 29 states. This 

finding led to 15 states imposing quarantines on nursery stock from California, 

resulting in estimated losses of $4.3 million to the nursery industry in California 

in the first month alone (Frankel 2008). The California Association of Nurseries 

and Garden Centers estimated that California nurseries lost $25 million in sales in 

spring 2004 when other states prohibited nursery shipments from California (US 

GAO 2006). In 2004, the U.S. Department of Agriculture Animal and Plant Health 

Inspection Service (USDA APHIS) spent approximately $20 million to trace and 

destroy all suspect stock from the two nurseries (Frankel 2008). Similar shipments 

of infested nursery stock, but at a smaller scale, occurred from Oregon and Washington nurseries. 

The potential loss to the nursery industry and forests in Oregon from P. ramorum was estimated to be between $81 million and $310 million per year (for direct 

control, management, and regulatory compliance costs plus loss of markets) (Cusak 

and others 2009, Griesbach 2008, Kanaskie and others 2008b, Oregon Invasive 

Species Council 2008). To comply with federal quarantine regulations, the Oregon 

Department of Agriculture (ODA) has spent about $3.2 million over a 5-year period 

(2001 through 2006) on surveys of nurseries for P. ramorum (Frankel 2008). In 

2007, the ODA needed to inspect over 1,450 nurseries to comply with the quarantine rules (Frankel 2008). 

Some of the financial impacts of P. ramorum in the nursery industry result 

from enforcement of regulations and other disease management practices to 

control pathogen spread. In fiscal year 2006, USDA APHIS estimated spending approximately $6.35 million in P. ramorum nursery activities in California, 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Oregon, and Washington. Approximately $4.15 million was allocated to inspection, 

sampling, testing, and certification activities. The remainder of the spending was 

allocated to national survey, trace-forward and trace-back investigations, eradication, and regulation enforcement activities (USDA APHIS 2007a). For Oregon nurseries, it was estimated that the cost of inspections and certification would increase 

from $800,000 to $6.5 million per year if the pathogen became widely established 

in the state (Griesbach 2008). If the disease became endemic in the Oregon nursery 

industry, Griesbach (2008) estimated that the annual cost of a prophylactic fungicide program targeted at P. ramorum would be $3,960 per acre (0.4 ha). Assuming 

that 10 percent of the 94,250 ac (38 141 ha) in production in Oregon opt for this 

treatment, the annual cost to the industry would be $37.3 million; if 25 percent of 

the area is treated, the cost increases to $93.3 million per year.

In addition to the monetary costs of compliance with federal quarantine regulations (compliance agreements and nursery and shipment certifications) borne by 

the public, the nursery industry has also incurred indirect regulation costs. For 

example, there could be potential costs associated with sales lost while withholding 

plants for shipment during inspection and testing (USDA APHIS 2007a). In Oregon, 

indirect costs owing to loss of sales from customer’s perception of the product being 

associated with or exposed to P. ramorum range from $34.1 to $204 million per 

year (Griesbach 2008). 

The number and retail value of plants destroyed in Washington state nurseries 

because of P. ramorum quarantine efforts between 2004 and 2005 were estimated 

by Dart and Chastagner (2007). Data collected during that period indicated that 

17,266 containerized nursery plants were destroyed at 32 nurseries, with an estimated retail value of $423,043. The mean loss per nursery was estimated at $11,188 

in 2004 and $11,798 in 2005. Other U.S. states do not record this information 

(Frankel 2008).

The presence of the pathogen within the nursery and ornamental trade has 

resulted in loss of markets. Oregon ships 75 percent of its nursery production to 

other states or countries (Griesbach 2008). In 2001, Canada closed its markets 

to most plant crops from the states of Oregon and California. Without reopened 

market access, Oregon nurseries alone faced losses in sales to Canada of $15 to $20 

million (Canada Gazette 2007, Frankel 2008). For the most part, Canada's markets 

were reopened to Oregon growers in 2002 (Regelbrugge 2003).

Additional losses to the nursery industry resulting from P. ramorum that have 

not been fully quantified include surveillance and testing costs, facility and equipment cleaning costs, costs of implementation of best management practices such as 

use of enzyme-linked immunosorbent assay prescreening tests, and others (Frankel 

2008, Sansford and others 2009, Suslow 2006).
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Nursery Industry, Canada and Europe

Resources at risk—

In Canada, the value of the British Columbia nursery and floriculture sectors was 

estimated at $500 million, with approximately $170 million in export sales to the 

United States (Canada Gazette 2007). Canada's export trade for rhododendrons was 

valued at $5 million in 2000 (Allen and others 2003).

Costs—

Costs to conduct required P. ramorum eradication work (plant destruction, soil 

treatment, loss of plant inventory) in British Columbia nurseries in the spring of 

2007 was estimated at $8.5 million. Since then, other nurseries have tested positive 

for the pathogen, which required additional eradication measures (Canada Gazette 

2007).

The current impact on nurseries in the European Union is considered to be 

moderate in terms of quality and control costs; including phytosanitary controls, 

the impact is major (Sansford and others 2009). The potential economic impact for 

the nursery trade in the European Union (27 member states) is estimated as high 

(Sansford and others 2009).

Cut Flowers/Foliage

Resources at risk—

Cut flower and foliage sales in the United States exceeded $406 and $542 million, 

respectively (Jerado 2007, as cited in Cave and others 2008). 

Costs—

Although the impact of P. ramorum to that industry has apparently been minor, 

Cave and others (2008) pointed out that there is an increase in flower production 

from woody ornamentals, and many of those plants are hosts for the pathogen, 

including Camellia, Hamamelis, Kalmia, Pieris, Rhododendron, Rosa, and Syringa

(Bachmann 2002). 

Environmental Impacts

The ability or potential of an introduced pathogen such as P. ramorum to cause 

environmental damage by disrupting native forest ecosystems is difficult to predict. 

The potential for environmental impacts to the nursery industry is equally difficult 

to estimate. Most literature describing environmental damage simply lists factors 

of the environment that could be affected, and then describes that environment. 

Factors typically considered under environmental damage include potential for 

ecosystem destabilization, reduction in biodiversity, reduction or elimination of 
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

keystone species, reduction or elimination of endangered or threatened species, and 

nontarget effects of control measures. 

The APHIS pest risk assessment for P. ramorum (Cave and others 2008), for 

example, rated the environmental impact of the pathogen as high based on three 

aspects: the potential of the pest to disrupt native ecosystems and habitats exhibited 

within its current geographic range; the need for additional chemical or biological 

control programs because of the presence of the pest; and the potential of the pest 

to directly or indirectly impact species listed as Threatened or Endangered (50 CFR 

§ 17.11-12). A high degree of uncertainty was assigned to the rating because of the 

difficulty in estimating costs that address all of the relevant ecological components, 

including the environmental costs of prevention, eradication, or suppression by 

herbicide use; the effects on endangered species and the indirect ecological consequences (changes in locally important ecological processes such as perturbations of 

hydrologic cycles such as flood control and water supply, waste assimilation, nutrient recycling, conservation and regeneration of soils, crop pollination, and habitat 

destruction) (Cave and others 2008).

Ecosystem Effects

Resources at risk—

Quercus spp. are considered the most important and widespread of the hardwood 

trees in the North Temperate Zone, with about 300 species (Pavlik and others 1991). 

Oak woodlands yield important benefits, including water and watershed protection, 

grazing, wildlife food and habitat, recreation, and wood products (Monahan and 

Koenig 2006, Thomas 1997). Oak species are part of forest and savanna woodland 

ecosystems in Europe and the United States (Global Invasive Species Specialist 

Group 2006).

Many of the foliar hosts of P. ramorum have ecological significance. Rhododendron spp. occur worldwide, and some species in the United States are currently 

listed under the Endangered Species Act. Vaccinium ovatum, native to British 

Columbia, Washington, Oregon, and California (Halverson 1986), is a prominent 

component of California and Oregon forests dominated by tanoak, canyon live 

oak (Quercus chrysolepis Liebm.) and Pacific madrone (Arbutus menziesii Pursh) 

(Sawyer and others 1977). Evergreen huckleberry is an important browse species 

for elk in the Coast Range and in southern Oregon. Vaccinium ovatum is closely 

related to blueberries and cranberries as well as other huckleberry species. All of 

the native huckleberries and blueberries are important to wildlife. The success and 

timing of berry crops has been tied to the reproductive rate of black bears, and berries are critical energy sources for Neotropical birds at the time of migration. The 
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plants themselves provide extensive cover for mammals and nesting birds as well as 

important winter browse. Vaccinium spp. are widely distributed throughout Europe, 

Asia, and North America; more than 40 species occur in North America.

Environmental and social benefits provided by U.K. woodlands/forests include 

open-access free recreation, landscape amenity, biodiversity, and carbon sequestration (Sansford and others 2009, Sansford and Woodhall 2007). Studies to assign 

values to these benefits and timber values for Great Britain were reviewed by 

Sansford and Woodhall (2007). The estimated social and environmental benefits 

of British forests (based on estimated values of the recreational and biodiversity 

benefits, landscape value, and carbon sequestration) are about £1,022 million per 

year (2003 figures). Adding the estimated timber value of British forests (about £36 

million), gives an estimated value of British forests of about £1,058 million per year 

(2003 figures).

Costs—

A major effect of P. ramorum in California coastal forests has been mortality of 

tanoak, coast live oak, and California black oak (Q. kelloggii Newberry). Meentemeyer and others (2008) estimated 235,678 trees (12 650 m2

 tree basal area) 

killed by P. ramorum in the Big Sur ecoregion (79 366 ha study area), of coastal 

California. The numbers represent about a 20-percent loss of available host trees. 

Nonlethal foliar and shoot infections occur on other susceptible forest species. The 

reduction of oak and tanoak populations in these forests has altered the forest stand 

structure and composition (Meentemeyer and others 2008c). The USDA FS risk 

assessment (Kliejunas 2003) pointed out that heavy loss of oaks, or of related susceptible genera, owing to P. ramorum infection could result in significant ecological 

effects, including changes in forest composition, loss of wildlife food and habitat, 

increased soil erosion, and a significant increase in fuel loads in heavily populated 

urban-forest interfaces. 

A pest risk assessment completed by the Plant Health Risk Assessment Unit of 

the Canadian Food Inspection Agency (CFIA) in March of 2002, and most recently 

revised in January 2008, concluded that the potential environmental impacts of P. 

ramorum on most areas of Canada is low. For south coastal British Columbia, the 

risk is medium (CFIA 2008).

In Europe, any significant loss of oak species to P. ramorum could impact 

soil erosion, hydrology, biodiversity, tourism, and cultural history (Global Invasive Species Specialist Group 2006, Sansford and others 2009). Other hosts of P. 

ramorum—European beech (Fagus sylvatica L.) and sweet chestnut (Castanea 

sativa Mill.) for example—are important high forest and plantation trees in Europe 

(Global Invasive Species Specialist Group 2006).
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

Although the potential effects of P. ramorum on rare and endangered plant 

species are unknown, Cave and others (2008) listed a number of genera on the 

APHIS List of Hosts and Associated Plants (Arctostaphylos confertiflora Eastw., 

A. glandulosa Eastw. ssp. crassifolia (Jeps.) Wells, A. hookeri G. Don ssp. ravenii

P.V. Wells, A. morroensis Wies. & Schreib., A. myrtifolia Parry, A. pallida Eastw., 

Prunus geniculata Harper, Q. hinckleyi C.H. Muller, and Rhododendron chapmanii 

Gray) that have species on the U.S. Fish and Wildlife Service (USFWS) Threatened 

and Endangered Species list. See http://www.fws.gov/endangered/wildlife.html for 

current listing of plants on the USFWS threatened and endangered list.

Recreational Effects

Resources at risk—

Urban and woodland areas affected by P. ramorum in California have many federal, 

state, county, and city parks and recreational facilities. Marin and Sonoma Counties 

are prime suburban and recreational areas. The economies of the Big Sur region and 

Santa Cruz are based largely on tourism and recreation. 

Costs—

Regulations and restrictions to prevent spread of P. ramorum affect recreational use 

of infested areas. Public access to areas may be restricted during certain seasons 

to prevent movement of the pathogen or to protect visitors from hazardous trees 

killed by P. ramorum. The Rogue River–Siskiyou National Forest in southern 

Oregon closed a popular trail just before Labor Day 2009 in response to detection 

of P. ramorum on a tanoak near the trail. Hazard tree removal from along trails in 

wilderness areas where chainsaws are prohibited would need to be done with handsaws, thus increasing costs; this also increases the likelihood of trail closures owing 

to a maintenance backlog in heavily impacted wilderness areas, such as the Ventana 

Wilderness on the Los Padres National Forest. When visitors are requested or 

required to take precautions to prevent movement of the pathogen, park and forest 

staff may be required to provide educational information, staff cleaning areas, and 

provide appropriate supplies and equipment to remove soil from shoes and vehicles 

(COMTF 2004c). Recreation may also be affected by a loss of recreational areas in 

woodland severely infested with P. ramorum (Appiah and others 2004). 

Wildlife Effects

Resources at risk—

Tanoaks and true oaks provide habitat and food for a variety of wildlife (Standiford 

2000). On the other hand, some small mammal species may benefit from loss 

of trees owing to P. ramorum. In California, dusky-footed woodrats (Neotoma
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GENERAL TECHNICAL REPORT PSW-GTR-234

fuscipes) were projected to benefit from the increased shrub cover, the California 

parasitic mouse (Peromyscus californicus) would benefit from an increase in 

coarse wood debris and the California brush mouse (P. boylii) would benefit from 

lower tree densities. Two salamander species—Monterey salamander (Ensatina 

eschscholtzii) and slender salamander (Batrachoseps spp.)—modeled were likely to 

be relatively unaffected (Tempel and Tietje 2006).

Costs—

Barrett and others (2006) indicated that the loss of L. densiflorus, Q. kelloggii, and 

Q. agrifolia would have negative effects on dozens of wildlife species because of 

the direct loss of these three forest tree species, and the associated loss of food and 

nesting and den sites. Northern spotted owls (Strix occidentalis caurina) are known 

to nest in tanoak stands in coastal California and Oregon, and when combined 

with an overstory of large conifers, a component of tanoak may improve habitat for 

the owls by providing canopy structure and habitat for prey such as wood rats and 

northern flying squirrels (Glaucomys sabrinus) (Niemiec and others 1995). A reduction of the oak overstory would also result in a more open canopy, which would 

encourage dense shrub cover. In studies on the effect of the disease on insectivorous 

cavity-nesting birds in stands of coast live oak in the San Francisco area, Apigian 

and Allen-Diaz (2006) observed a loss of bird nest sites, prey reduction, and loss 

of foraging substrates in P. ramorum-affected plots. Monahan and Koenig (2006) 

reported a negative impact on populations of five California bird species associated 

with coast live oak in California. The authors projected that bird populations could 

be 25 to 68 percent smaller and 13 to 49 percent more variable in infested stands 

compared to noninfested stands. The greater number of beetles associated with 

infected trees (McPherson and others 2005) may also affect the feeding patterns of 

birds. 

Fischer and Hadj-Chikh (n.d.) used regional risk models for P. ramorum to 

determine risk of habitat infestation to special status vertebrates in California, 

Oregon, and Washington. In California, seven amphibians, five birds, seven mammals, and one reptile had more than one-third of their predicted habitat at risk of 

infestation. The numbers for Oregon were 15 amphibians, 18 birds, 21 mammals, 

and 2 reptiles; and for Washington, 18 amphibians, 139 birds, 58 mammals, and 16 

reptiles.

Program Costs

Government

United States Federal Agency expenditures on P. ramorum regulatory, research, 

management, and related activities from 2000 to 2009 were APHIS, $61 million; 
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USDA FS, $39.9 million; Agricultural Research Service (ARS), $11.9 million; and 

Cooperative State Research, Education and Extension Service (CSREES), $1 million (Frankel 2009).

As stated previously, the U.K. Environment Minister will provide £25 million 

over 5 years (2009 through 2013) to help contain and eradicate P. ramorum and P. 

kernoviae from historical gardens, woodlands, heathlands, nurseries, and retailers 

in England and Wales. 

Other

Other expenditures for P. ramorum include funds from the states of California, 

Oregon, and other states for education; state and federal salaries for researchers and 

forest health protection personnel; private grant and nonprofit funds (for example, 

the Moore Foundation, Oregon Association of Nurseries, other nursery organizations, the Nature Conservancy); and others.

Summary

The current and estimated potential economic and environmental impacts of P. 

ramorum indicate a significant effect of the introduced pathogen. Current economic 

impacts to forests/woodlands have occurred primarily in central coastal California and southwestern Oregon. Economic losses there have been minor, as host 

mortality occurs primarily in nontimber species. Current economic impacts in the 

European Union are estimated as minor to moderate. Potential economic losses 

have been estimated to be much greater if the pathogen becomes established in 

other areas, in particular the commercial forests of the Northwest or Eastern United 

States. Economic impacts in urban areas include reduction in property value and 

costs associated with hazard tree removal and fire management. Current economic 

impacts to the nursery/ornamental industry in the United States are estimated to be 

in the range of $100 to $300 million. Canada spent about $8.5 million in 1 year on 

control. Estimated impacts if the pathogen spreads are much higher.

Environmental impacts from P. ramorum are not fully known because the 

introduced pathogen has been affecting forest ecosystems only since the mid-1990s 

and the nursery industry for less time. Estimates of potential environmental impacts 

range widely (spanning several orders of magnitude), depending on assumptions 

made. The potential for P. ramorum to impact ecosystems depends on numerous 

factors, many of which are presently unknown.

Although the benefits and costs of various management scenarios have been 

estimated (see Hall and Albers 2009, and Friend 2008, for example), a comprehensive cost-benefit analysis of the disease has not been done.
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Acknowledgments

Thanks to Douglas McCreary, University of California Center for Forestry and 

Integrated Hardwood Range Management Program, for administrative support. 

Thanks also for the review and guidance provided by Susan Frankel, USDA Forest Service, Pacific Southwest Research Station; Everett Hansen, Oregon State 

University; David Rizzo, University of California-Davis; Alan Inman, UK Food 

and Environment Research Agency; Ellen Goheen, USDA Forest Service, Forest 

Health Protection; Jonathan Jones and Glen Fowler, USDA Animal and Plant Health 

Inspection Service; and Ross Meentemeyer, University of North Carolina, Charlotte. 

Funding was provided by the USDA Forest Service, Pacific Southwest Research 

Station, Sudden Oak Death/Phytophthora ramorum Research program. 

English Equivalents

When you know: Multiply by: To find:

Micrometers (μm) 0.000039 Inches

Millimeters (mm) 0.0394 Inches

Centimeters (cm) 0.394 Inches

Meters (m) 3.28 Feet

Kilometers (km) 0.6215 Miles

Square meters (m2) 10.76 Square feet (ft2)

Square kilometers (km2) 0.386 Square miles (mi2)

Hectares (ha) 2.47 Acres (ac)

Cubic meters (m3) 35.314 Cubic feet (ft3)

Kilograms per hectare (kg/ha) 0.893 Pounds per acre (lb/ac)

Milligrams per kilogram (mg/kg) 1 Parts per million (ppm)

KiloPascal (kPa) 0.145 Poundforce per square 

 inch (lbf/in2)

Degrees Celsius (oC) 1.8 and add 32 Degrees Fahrenheit
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Sudden Oak Death and Phythophthora ramorum: A Summary of the Literature—2010 Edition

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