On a warm, sunny September afternoon, Ted Swiecki and Elizabeth Bernhardt stepped out of a silver SUV in the parking lot of Skyline Ridge Open Space Preserve in search of a killer.
After unloading their gear -- a shovel, surgical gloves, a camera, plastic bags and surveyor's tape -- the pair trudged through native bunchgrass, oak forests and shrubs, carefully tracking their coordinates on an iPad and smartphone.
Plant pathologists from Phytosphere Research in Vacaville, Swiecki and Bernhardt are detectives of the plant world, and recently, they've been searching for the origin of a deadly disease that has been plaguing plants high above Silicon Valley. Phytophthora (fie-TOF-thora), a fungus-like water mold whose name means "plant destroyer," is every bit as deadly as it sounds.
Experts worry that it could wipe out whole populations of plants and change entire ecosystems. By some research estimates, there are more than 100 known species of the pathogen worldwide. Swiecki and Bernhardt have identified at least 60 forms of Phytophthora in nursery-grown native plants. (Read "A plant killer with huge economic impact")
About a half-dozen or so species have been found in various wildland locations, Swiecki said.
"All evidence indciates that these are all introduced species," he added.
The pathogens are not native to the U.S.; they hitchhiked in on plants brought from overseas, including Asia and parts of Europe. The deadly water molds attack with ferocity precisely because California's native plants have little resistance, said Swiecki and Bernhardt, who are Phytophthora experts.
The variety that attacks plants' roots chokes off a plant's ability to take up nutrients and water, Swiecki said. There is another kind that spreads by leaves and causes the more-well-known sudden oak death.
A recent infestation was found in Monte Bello Open Space Preserve, along Page Mill Road, which is why Swiecki and Bernhardt have come to Skyline Preserve, located across Skyline Boulevard from Monte Bello. Valley oaks, toyon and madrone in Monte Bello have been infected with Phytophthora cambivora, the root-rotting form. The pair suspect Phytophthora might have spread to Monte Bello from Skyline Preserve.
The site slopes down gently from Skyline's 2,100 to 2,200 feet of elevation to 1,600 feet in Monte Bello. The water molds could be carried by Stevens Creek or by water moving through the soil, they said. Research indicates that Phytophthoras have been found in creeks in other locations.
Swiecki and Bernhardt have zeroed in on this particular area of Skyline because Midpeninsula Regional Open Space District, which owns the land, replanted part of the area with toyons, oaks and madrones nearly 10 years ago. If the infestation came from these plants, there would be signs. More difficult to prove but not less troubling, crews might have brought the disease in -- or spread it -- on equipment, boots or shovels. Anything that might collect bits of soil or plant material could carry the disease, they said. Swiecki pointed south to a verdant area of conifers. Phytophthora might also have come from a nearby Christmas tree farm, where it may have resided for decades, he said.
Bernhardt worked her way up the slope, inspecting planted trees and shrubs encircled by wire cages. She looked for openings where wildlife might have entered or deer might have browsed, explanations for why the plants appeared stunted. But the cages were secure, the leaves unnibbled.
Swiecki began digging around the roots of a toyon, the berries of which many birds eat. To the untrained eye, the plant appeared healthy. But Swiecki and Bernhardt recognized signs of possible Phytophthora infection. The leaves were chlorotic, a paler green or even yellowish, which is not normal, and the leaves were about half the size they should have been.
The plant was also only about 3 feet tall.
"These toyons are not dead, but they are 10-year-old plantings. They should be over my head," Swiecki said.
He rocked the shovel back and forth, chipping away at the layers of hardened earth. He found telltale signs of planting by humans: lava rock and Perlite, which are never found in the wild, he said. When he got to the root ball, Swiecki noticed the trunk base was misshapen. The roots also were not very widespread.
"Very limited root density is an indicator of Phytophthora," he said.
A drought, however, also causes trees and shrubs to produce fewer new roots, which means that some plants infected with Phytophthora, which makes plants look water-starved, could be overlooked.
Swiecki used a hand trowel to dig out roots and soil, depositing a shovelful in a plastic bag. Before they left, Swiecki whipped out a spray bottle containing rubbing alcohol that he keeps attached to his belt. He sprayed every surface of the shovel and other implements to disinfect them before moving on.
Further up the slope Bernhardt located a small madrone tree no larger than a small bush. The red-bark trees are an important source of food for many birds, who also nest in them. The top was dry, a russet-orange color, and drooped over. Swiecki said this kind of crown death is characteristic of Phytophthora infections. Nearby, a small planted oak in a cage had died completely. Its tan, papery leaves looked as though they had dried out all at once.
Swiecki and Bernhardt focused on another troubling sign. A madrone that had not been planted had the same russet-orange color. It was almost entirely dead, except for a very slight tinge of yellow-green on the leaf undersides. If this plant proved to be infested with Phytophthora, it could indicate that the disease had spread into the wildland from the plantings. Swiecki again dug down for samples; Bernhardt tied surveyor's tape to the branches to mark the tree. Swiecki searched the area for other possible sources of contamination.
"It's next to erosion-control material. There are a lot of different possible sources here," he said.
Down in Silicon Valley, another species of Phytophthora that likely arrived on nursery plants is stalking the urban forest.
On the campuses of Brentwood Academy and McNair Elementary School in East Palo Alto, weeping cankers ooze sap, forming dark lesions on the trunks of cork oaks. Canopy, the Palo Alto nonprofit, has planted these and hundreds of other trees throughout East Palo Alto, along with thousands in Palo Alto, over the years to help beautify the communities.
When staff noticed the oozing trunks, they called in Igor Lacan, urban horticulture advisor for U.C. Cooperative Extension San Mateo-San Francisco Counties, to sample the ooze. Lab results showed the disease to be Phytophthora cinnamomi, a pervasive species that has been found in at least 70 countries.
Michael Hawkins, Canopy program director and a certified arborist, said the trees were planted in 2012; about a dozen at each school showed signs of bleeding cankers two summers ago. The trees were purchased from a nursery that was most likely the source of the outbreak. They looked healthy when they were planted, but after a time, when they were watered, the cankers began to form, he said.
Hawkins said Canopy moved irrigation further away from the affected tree trunks and replanted some trees. The trees were treated with chemicals recommended by the nursery: phosphite, a phosphorus compound, and Subdue Maxx, which fights fungus in the roots. But while those measures have helped to lessen the symptoms, the name of the treatment perhaps says it all: It subdues the Phytophthora but does not eliminate it.
Swiecki said that nurseries routinely use fungicides, which suppress the disease, but once the plants are in the field and the fungicide is no longer applied, the disease comes roaring back.
That's a scary scenario for land managers of open space areas. Unless every plant was individually tested before going into the ground -- an impossibly expensive proposition -- it is probable that many thousands of infected plants are being released into the wild through restoration projects and by residents who live near the urban-wildland interface and near creeks
No one would know it until the plants die. That's what happened in the San Francisco Public Utilities Commission (SFPUC) Peninsula watershed in San Mateo County, and in parts of Santa Clara Valley Water District's watershed.
Large restoration projects by SFPUC in its watersheds were supposed to mitigate habitat destruction caused by upgrades to the Hetch Hetchy Regional Water System. But when a planted toyon showed the characteristic dead leaves, Greg Lyman of SFPUC's natural resources land management division took the plant to Swiecki for testing, Lyman recalled during a 2014 lecture.
Swiecki used a simple test, using a green pear to cultivate the pathogen. Water percolated through the soil and the root system of a suspect plant is collected, and the pear is placed in the bath. Rot on the pear is an indication of the disease, which is then cultured and examined at the Rizzo Lab at the University of California Davis, which is run by David Rizzo.
Swiecki came back with sobering news.
"This plant is hot," he told Lyman.
"That pear was brown," Lyman said.
The plant tested positive for Phytophthora tentaculata, which is one of two species on the U.S. Department of Agriculture's quarantine list, with a potential to decimate many cultivated crops as well as native species. Phytophthora tentaculata was not previously known in the U.S. until it made its appearance in 2014 at a nursery in Monterey County.
SFPUC also discovered it had planted infected material from multiple nurseries with 10 species of Phytophthora. Phytophthora cinnamomi, the one found on Canopy's cork oaks, was also found spread into the SFPUC Peninsula watershed on madrone and bay laurel trees.
The costs could be enormous. SFPUC received about 500,000 plants for its two watersheds. How many of those plants might be infested is still a question that only time will reveal. Many native plants, because they are drought resistant, might not show outward signs of the diseases for some time, while the micro-organisms continue to proliferate and spread.
"Our concern is that we've introduced a pathogen into the watershed that could decimate a whole ecosystem," Lyman said.
Trying to stem the spread of these pathogens is a costly proposition: If the SFPUC restoration fails because of Phytophthora, the restoration will have to start from scratch, Lyman said. The cost could be as high as $45 million for obtaining new stock and planting alone. Testing and treatment has cost $700,000 and is growing. (Read "Vigilance can prevent spread of Phytophthora")
Santa Clara Valley Water District was also faced with a similar problem in 2014 when all of the plants of its rare Coyote ceanothus restoration project died. The entire pilot project at Coyote Ridge in the Mt. Hamilton Range was infected with Phytophthora cactorum. A riparian revegetation project at Guadalupe Creek in downtown San Jose was initially found to have Phytophthora tentaculata, then 14 additional species of the micro-organisms were found, including another high-risk species, Phytophthora quercina, which along with tentaculata is in the top five Phytophthora species of concern by the U.S. Department of Agriculture.
Ngoc Nguyen, interim deputy operating officer for district watersheds, said that all 240 plants from a local native plant nursery did not survive shortly after planting. Staff removed them all and determined that the infestation had not spread, and they are now heat-treating the soil at each spot.
Phytophthora can live in the soil undetected for many years, waiting for opportune conditions to maximize its spread. Multiple species have been found at Filoli Estate in Woodside, which has its own nursery. There is evidence that the pathogens spread to areas outside of the nursery along Cañada Road, most likely from the nursery, Swiecki said. In San Francisco's Golden Gate Park, the site of a nursery that had been abandoned for 50 years also tested positive for Phytophthora.
On water district land near Anderson Dam in southern Santa Clara County, staff made a startling discovery. A 20-year-old restoration planting revealed active Phytophthora cactorum on rare Coyote ceanothus. The entire planting was uniformly infected, said Cindy Roessler, senior resource management specialist at Midpeninsula Regional Open Space District, who worked for the water district at the time. Roessler thinks the infection came in on the nursery plants.
The experience has been "humbling," she said.
But there have also been mysterious contaminations of nurseries from plant material collected in the wild. At Mt. Umunhum, another Midpeninsula Regional Open Space acquisition, members of Grassroots Ecology, a nonprofit nursery in Palo Alto's Foothills Park, collected stock of spike moss, a ground cover, to grow at the nursery for the open space district.
But when the plants looked suspect, the nursery collected water draining from the pots and set a green pear in it. The pear developed brown spots, which tested positive for Phytophthora cambivora. The nursery pulled all of the plants and put them in quarantine, and ultimately had to destroy them, said Nikki Hanson, the nursery manager.
The source of the contamination has not yet been identified, but Roessler said heavy moving equipment at the site might have played a role.
The district is now taking a cautious approach. Roessler suspended using any nursery stock in the district's preserves and instead is directly sowing seeds. The district is spacing plants farther apart, and at Umunhum the district is planting 50 micro-sites to see how new plants respond before expanding the project.
Roessler is co-chair of the restoration committee of the Phytophthoras in Native Habitats Work Group (CalPhytos.org), an organization that includes researchers, state and federal agencies and land managers. The group is working on protocols for best management practices and inspection of nurseries. Grassroots Ecology's nursery is following "best management practices" being developed by a Phytophthora task force, and it now has two new greenhouses -- one dedicated for Midpen projects and the other for water district grow outs. (Read "Native-plant nurseries seek to combat Phytophthora")
A pilot program to develop Phytophthora-free certification for nurseries is also underway. Susan Frankel, a U.S. Forest Service Pacific Southwest Research Station plant pathologist and a co-leader of the habitats work group, said the project will set up an accreditation checklist of phytosanitary (plant cleanliness) measures, and it will take samples from nurseries to track pathogens and whether the practices are effective. A plant pathologist will work with nurseries to tailor the practices to the nursery and make sure they are practical but effective. Then an inspector will check periodically to monitor that the practices are being followed.
So far, seven Bay Area nurseries have agreed to take part in the pilot project, which will include a range of nursery sizes and types of operations, such as those using volunteer labor or professional staff. Which agency would do the certification hasn't yet been decided, she said.
Swiecki said that it's important for nurseries -- and the public -- to become aware of the problem and its potential to harm the environment. His work with the Ione manzanita, a threatened species, has shown how devastating Phytophthora can be. Wide swaths of the shrub have been wiped out.
But that isn't all. Phytophthoras are attacking forests in Oakland and Sonoma and other parts of the Bay Area, and they aren't limited to trees. Water-loving Phytophthora species also attack aquatic plants. A cross of Phytophthora inundata was discovered in the marshes in lower San Francisco Bay, and it is attacking the pickleweed in a site that was being mitigated for the Salt Marsh harvest mouse. And sages, sticky monkey flower, coffeeberry, Artemisia, coyote mint and many other plants are susceptible to Phytophthora species. The Rizzo Lab in 2016 identified the microbes on about 30 native plant species planted from nursery stock.
While the root-rotting forms are currently in small areas, one need look no further than what another infamous Phytophtora species has already accomplished.
Sudden oak death from Phytophthora ramorum, which attacks the leaves of trees, has killed more than 3 million oaks in California, according to the task force. It has caused twig and leaf diseases in many other plant species, including California bay laurel, Douglas fir, and coast redwood, according to the California Oak Mortality Task Force.
Identified 30 years ago, it was not a widely damaging pathogen until 2004, when a few large West Coast nurseries inadvertently shipped more than 1 million potentially infected ornamental rhododendrons and camellia plants throughout the U.S. Now it has spread to 21 states. Its origin is not known.