A Short Course Presented by the California Oak Mortality Task Force Phytophthora ramorum A Short Course Presented by the California Oak Mortality Task Force Part 1 - Introduction to Phytophthora ramorum and Sudden Oak Death Background Photo Credits: Karl Buermeyer, UC Cooperative Extension (forest scene) Jan Hedberg, Oregon Department of Agriculture (viburnums in nursery) Steve Tjosvold, UC Cooperative Extension (rhododendron)

Course Outline Part 1 - Introduction to Phytophthora ramorum and Sudden Oak Death History Biology Impacts - Past, Present, and Future Review Questions Part 2 - Symptom Recognition, Diagnosis, and Sampling Part 3 - Regulations and Management of Phytophthora ramorum

Part 1 - Introduction to Phytophthora ramorum and Sudden Oak Death History In the mid-1990s, large numbers of tanoaks and coast live oaks began to die in the coastal counties of central California. The cause of death was unknown, and due to the rapid browning of the foliage, the condition was named “Sudden Oak Death.”

Rizzo Lab, UC Davis In July 2000, scientists discovered the cause of Sudden Oak Death to be a newly identified species of Phytophthora. This pathogen was the same as one that had been observed on rhododendrons and viburnums in nurseries and gardens in Europe since 1993. The new species was named Phytophthora ramorum.

Distribution List as of April 2006 As of April 2006, U.S. wildland Phytophthora ramorum infestations have been confirmed in 14 California counties and Curry County, Oregon. Once considered only a forest disease in North America, nursery detections are now made annually in dozens of nurseries throughout the nation. Distribution List as of April 2006

From 1993 to 2003, Phytophthora ramorum in Europe appeared to be limited to nursery and garden situations. Affected countries included Belgium, Denmark, France, Germany, the Netherlands, Norway, Poland, Republic of Ireland, Slovenia, Spain, Sweden, and the UK. Plant Protection Service, The Netherlands, 2003 However, in the fall of 2003, several tree species in the Netherlands and UK that were adjacent to diseased rhododendrons became infected. Along with the increasing number of nursery finds in North America, this raised concern that nursery host movement and out-planting could facilitate long-distance pathogen spread to previously uninfested locations.

Biology Jennifer Parke, Oregon State University Phytophthora ramorum belongs in the kingdom Chromista (Stramenopiles), and is related to diatoms and brown algae. The genus Phytophthora (“plant destroyer”) has more than 60 species, many of which are virulent plant pathogens. They are Oomycetes, or “water molds;” water is crucial to their lifecycle and management. Phytophthora ramorum is microscopic. It develops hyphae (collectively called mycelium), which grow through bark and leaf tissue. It also produces asexual reproductive structures called sporangia and chlamydospores. Sporangia release zoospores which have two flagella that propel them through water. Chlamydospores are hardy structures that protect the pathogen during adverse conditions, such as heat and drought, but little is known about their role in disease progression or the conditions leading to their germination. Rizzo Lab, UC Davis

Phytophthora ramorum is heterothallic; it requires two different mating types (A1 and A2) for sexual reproduction through structures called oospores. In Europe, the Phytophthora ramorum population is primarily the A1 mating type. While only the A2 mating type is found in North America, the European A1 mating type has been intercepted and destroyed in a small number of Pacific Northwest nurseries. So, while sexual reproduction has not been observed outside of the laboratory, there is concern about the two mating types coexisting in nature, as sexual reproduction could occur and potentially produce more virulent and adaptable pathogen strains.

Phytophthora ramorum grows and sporulates on the surface of leaves and twigs of a number of plant species known as “foliar hosts.” It can also grow into the cambium and outer xylem of “bark hosts” and effectively girdle the tree; this is “Sudden Oak Death.” Thus, the same pathogen causes two different diseases. Slide 10 is a list of the known Phytophthora ramorum hosts. Plants that may be killed by the pathogen are underlined. There are numerous species, hybrids, and cultivars of ornamental plants that have been found to be infected by Phytophthora ramorum. For a complete up-to-date list by species and hybrids (not cultivars), consult the California Oak Mortality Task Force website: www.suddenoakdeath.org.

Host Species, part I California bay laurel California black oak Canyon live oak Coast live oak Coast redwood Douglas-fir European yew Holm oak Shreve’s oak Southern red oak White fir Grand fir Red fir Striped bark maple Evergreen maple Planetree maple Horse chestnut Portuguese laurel cherry European turkey oak Sessile oak Northern red oak Pacific yew Yew California nutmeg Strawberry tree Sweet chestnut Winter’s bark European beech Bigleaf maple California buckeye Madrone Oregon ash Bay laurel Southern magnolia Star magnolia Loebner magnolia Saucer magnolia Michelia doltsopa Michelia maudiae Michelia wilsonii Roble beech Victorian box Cascara European ash Griselinia Tanoak Persian ironwood Continued on next slide…

Host Species, part II Rugosa rose California hazelnut Salmonberry Arctostaphylos columbiana Arctostaphylos manzanita Western maidenhair fern California maidenhair fern Scotch heather Camellia spp. California coffeeberry Witch hazel Toyon California honeysuckle False Solomon’s seal Red tip photinia Mountain Andromeda Himalaya Andromeda Japanese Pieris Formosa firethorn Rosa ‘Meidiland’ Vine maple Rugosa rose Salmonberry Goat willow Poison oak Redwood ivy David Viburnum Fragrant Viburnum Wayfaringtree Viburnum European cranberrybush Viburnum Burkwood Viburnum Prague Viburnum Alleghany Viburnum Ardisia Spicebush Andrew’s clintonia bead lily Laurustinus California hazelnut California wood fern Spreading euonymus Salal Hybrid witchhazel Chinese witchhazel Mountain laurel Fetterbush Drooping leucothoe Sweet Cicely Osmanthus Rhododendron spp. Wood rose Lilac Western starflower Evergreen huckleberry Bodnant Viburnum Doublefile Viburnum Host List as of April 2006

The pathogen spreads primarily through sporulation on leaves and twigs of foliar hosts; little sporulation has been observed in bark hosts. So, although infections may not cause significant damage to foliar hosts, they are vital to the life cycle and spread of the pathogen. Phytophthora ramorum exists within a temperature range of 36 to 80°F, with an optimum temperature of 68°F. Spore structures form on foliar hosts in as little as 24 hours after a wet period. Spores are then transported in water droplets to the soil, the bark of surrounding trees, and other leaves. In California, the organism sporulates prolifically on California bay laurel (Umbellularia californica). Host plant proximity to infected California bay laurel is considered the highest risk factor for infection. Steve Tjosvold, UC Cooperative Extension, 2004

Impacts of Phytophthora ramorum-caused diseases Karl Buermeyer, UC Cooperative Extension, 2002 Since it was first noticed, Sudden Oak Death has caused the death of tens of thousands of tanoaks and true oaks. The disease has impacted California coastal evergreen forests, redwood forests with tanoak understories, and tanoak-dominated forests in Oregon. Preliminary research indicates that resistance to the disease is present in all bark hosts, but more so in coast live oak than in tanoak. In limited populations of tanoak that are geographically isolated, almost total mortality has been observed. The spread of Phytophthora ramorum in natural situations appears to be limited to moist climates with moderate temperatures and the presence of foliar hosts. Yet, nurseries create their own environmental conditions and grow host species that would not naturally occur in the surrounding environs. Therefore, nursery infestations are not limited to naturally infested regions.

Long-term wildland impacts may include: Visual impacts from dead trees and altered forest canopies Altered ecosystems due to loss of important trees Increased fire hazard from dead, woody material Shortages of food and habitat for wildlife Water quality impacts from loss of shade and increased run-off Financial impacts of mitigation and quarantine efforts Karl Buermeyer, UC Cooperative Extension, 2004 Homeowners in urban/wildland interface areas have suffered aesthetic and property value loss as landscape trees have been killed. These trees can become hazardous in a matter of months, due to failures resulting from decomposition by secondary insect and fungal organisms. Homeowners or public agencies incur substantial costs to remove these trees.

Phytophthora ramorum nursery and plant The recent increase in nursery infestations has greatly impacted the nursery industry in Europe, Canada, and the U.S. monetary impacts include: Phytophthora ramorum nursery and plant shipment inspections, and disruption of shipment schedules The implementation of mitigation measures The destruction of plants in infected nurseries Loss of export potential due to quarantines Canadian Food Inspection Agency, 2003 Trees close to infected rhododendron plantings in European gardens recently became infected by Phytophthora ramorum, demonstrating the potential for the pathogen to spread through the nursery trade and into natural settings. Two species infected in this way were northern red oak (Quercus rubra) and southern red oak (Q. falcata). Both are native to the eastern U.S. and grow in forests with foliar host understories, such as rhododendron and mountain laurel, in climates favorable to Phytophthora ramorum. Other infected species, such as European beech (Fagus sylvatica) and horsechestnut (Aesculus hippocastanum) are commonly planted as ornamentals worldwide.

Review Questions 1. Phytophthora ramorum causes two basic diseases. What are they? Bark cankers on oaks, tanoaks, and other trees (“Sudden Oak Death”); Foliar and twig blight on a number of other plants from a wide range of families (“Ramorum Blight”) 2. What environmental conditions are most favorable for the spread and survival of Phytophthora ramorum? Moderate temperatures (~68° F) with ample moisture 3. What tree species most readily succumbs to P. ramorum? Tanoak (Lithocarpus densiflora)

Review Questions, continued 4. What is the biggest concern about Phytophthora ramorum in nurseries? It is a potential vector for long-distance spread of the disease into wildlands 5. What limits the genetic diversity and adaptability of Phytophthora ramorum? Lack of sexual reproduction 6. Why does Phytophthora ramorum do poorly in dry conditions? Free water is needed for spores to develop and move

Review Questions, continued 7. What costs, specific to the nursery industry, have been incurred as the result of Phytophthora ramorum? Implementation of inspections and mitigation measures Loss of export markets Destruction of infected plant blocks 8. Why is the eastern U.S. considered a risk for natural infestations of Phytophthora ramorum? There are susceptible red oak species with foliar host understories 9. Why is Phytophthora ramorum not as geographically limited in nurseries as in wildlands? Nurseries create their own climatic conditions and host species distribution