Urgent!! Send Comments to California on risk from new Phytophthoras

Arctostaphylos uva-ursi (bear berry); photo by Sten Porse, Commons.Wikipedia

The California Department of Food and Agriculture (CDFA) is seeking input on proposed pest ratings for two species of Phytophthora: Phytophthora occultans and Phytophthora quercetorum. Each has the potential for being a serious pest in California and being spread throughout the United States. Therefore it is important to weigh in on this process. The first deadlines for comments is December 18.

These risk rating proposals can be found at https://blogs.cdfa.ca.gov/Section3162/ The website also has instructions for sending comments. This process can be clumsy so, if it doesn’t work, send your comments directly to the webmaster.

In general, the State assigns each potential pest a rating of A, B, or C. Those rated “A” are most likely to cause harm and also most subject to State regulation. Under “B”, the County Agricultural Commissioners have discretion to take regulatory actions. Pests ranked at “C “are not subject to any State enforced regulatory actions. The “C” rating is supposed to be assigned to pests that are widely distributed in the state and are expected to have a “medium” to “low” impact on vegetation (cultivated or wild) in the state.

Phytophthora occultans

Proposed for risk rank “C “. Comments are due December 18th.

Phytophthora occultans is a recently described species found in nurseries in Europe and in some U.S. states (including Oregon). It was recently detected in the San Francisco area of California.

The State proposes to rate  Phytophthora occultans as a level  “C” pest. This is insufficient. A rank of “B” is more appropriate, for the following reasons.

1) The data presented in the CDFA proposal are too limited to judge the species’ distribution in California. The proposal refers to only “two detections, two years apart, in San Francisco County.” By ranking it “C”, CDFA seems to assume the pathogen is widespread, based on detections in Europe and other states, without U.S. evidence

The available record does not indicate that CDFA made any attempt to determine the extent of the P.occultans infestations — no survey of other plants at the contractor’s nursery or at other nurseries and no consultation with a larger group of stakeholders. 

2) CDFA limits discussion of possible impacts to hosts listed in the literature –which belong to multiple plant families. It makes no mention that additional hosts are likely to be discovered (as has often happened with regard to the host ranges of other pathogens in the Phytophthora genus).  If the host range expands, as I expect it will, the impact to restoration activities, rare plants, wildlands and nurseries is more likely to be significant, not medium to low. 

Furthermore, several of the known host species are congeners of species that are federally listed as endangered or threatened, i.e., species in the genera Ceanothus and Arctostaphylos. I think it is highly unwise to disregard in risk assessments the probability that listed species will prove to be hosts.

In conclusion, please submit comments to California Department of Food and Agriculture urging it to assign a risk rating of “B” to Phytophthora occultans.

Phytophthora quercetorum

Proposed for risk rank “C “. Comments are due January 9th. See https://blogs.cdfa.ca.gov/Section3162/

Instructions are contained in the proposal. If this process doesn’t work (sometimes it is clumsy), send your comments directly to the webmaster.

Over the past 5 years, P. quercetorum has been detected in association with oak trees, primarily coast live oak (Quercus agrifolia), in four counties in California, two in the Central Valley (Fresno, Sacramento), two on either side of the San Francisco Bay (Alameda, San Francisco). There have been no interceptions of the species by CDFA border inspectors. The species had earlier been associated with oak roots and rhizosphere soil of oak forests in the eastern and north central US. Its pathogenicity is said to be unknown – and difficult to separate from impacts of other, often co-occuring Phytophthoras. CDFA assigns a rank of “high” with regard to economic impact, although it says there are no reports quantifying economic losses in plant production facilities.

CDFA believes that the species is likely to be able to establish wherever its hosts can grow (a rank of “high”). Hosts include red maple (Acer rubrum), English ivy (Hedera helix), several eastern oaks, and a second California oak, interior live oak (Q. wislizeni). CDFA assigns this a rank of “moderate” host range.

The environmental impact is ranked as “high” since the pest could lower biodiversity, disrupt natural communities, or change ecosystem processes; and the pest significantly impacts cultural practices, home/urban gardening or ornamental plantings.

The overall ranking for the “Consequences of Introduction” is “high”.

However, the recommended ranking is “C”, which – again – means the pest is not subject to any State enforced regulatory actions. “C” rated pests are widely distributed in the state and are expected to have a “medium” to “low” impact on vegetation (cultivated or wild) in the state.

Why would CDFA recommend “no action” for yet another Phytophthora species that is known to attack two of the state’s most ecologically important oaks and possibly many more species? Even when the exact impacts are unclear … Especially when the principal means of spread is planting trees in restoration areas – a deliberate human action.

According to the USDA Forest Service, coast live oak (Quercus agrifolia) is a conspicuous tree in lower-elevation oak woodlands of California, which collectively occupy about 10 million. It is co-dominant in the southern oak woodlands. CLO trees generally occur on mesic sites such as north slopes, alluvial terraces, canyon bottoms, or upper streambanks. Coast live oak woodlands are some of the most important habitats to wildlife in California; they provide habitat for black bear, black-tailed deer, rodents and lagomorphs, and various upland game and nongame birds – including those that feed on acorns and cavity nesters. The birds including the federally endangered least Bell’s vireo and least tern.  

Coast live oak is more fire resistant than other California oak species. 

Coast live oak is favored for use in rehabilitation projects throughout its range. It is used in watershed improvement, restoration, and wildlife habitat rehabilitation projects.

CLO is already under pressure by predation by deer and cattle; sudden oak death (SOD; causal agent Phytophthora ramorum); goldspotted oak borer (GSOB – Agrilus auroguttatus); and sometimes the polyphagous shot hole borer (PSHB; Euwallacea whitfordiodendrus) and its associated Fusarium fungus. [These three non-native organisms are described here.]

range of Q. wislizeni; USDA Forest Service map

According to the USDA Forest Service, interior live oak (Quercus wislizeni) occurs over about 16% of California’s landscape, especially in the Inner Coast Ranges, the foothills of the southern Cascade Range, and the Sierra Nevada. Among California’s red oaks, interior live oak has the highest tolerance for xeric conditions. It usually dominates the “scrub” or “live oak” chaparral vegetation types in the Inner Coast Ranges and the Sierra Nevada.

CNPS Calscape lists several insects associated with the species.

Posted by Faith Campbell

We welcome comments that supplement or correct factual information, suggest new approaches, or promote thoughtful consideration. We post comments that disagree with us — but not those we judge to be not civil or inflammatory.

For a detailed discussion of the policies and practices that have allowed these pests to enter and spread – and that do not promote effective restoration strategies – review the Fading Forests report at http://treeimprovement.utk.edu/FadingForests.htm

SOD – Regulations Should Reflect Disease’s Complexity

Syringa vulgaris Chmurka 2018-05-06 1352.jpg Wikimedia Commons

As we know, the SOD pathogen Phytophthora ramorum infects more than 100 plant species [APHIS host list posted here]. Some are killed, some not. Some support production of spores (=sporulation), and thus promote spread of the disease – either in nurseries and plantings, or in the wild. Conditions under which P. ramorum infects specific plant species also varies.

In both the ornamental plant industry and natural environments, transmission is driven mostly by foliar hosts.

Matteo Garbelotto and colleagues have carried out studies aimed at improving our understanding of the differences in host-pathogen interactions, and their meaning vis a vis persistence and spread of the disease – especially in wildland situations. The experiments were carried out five or more years ago, funded by the Farm bill Section 7721 funding. See the full reference at the end of this blog.

The team ranked 25 ornamental plant species representing ten families for susceptibility to P. ramorum and infectivity (spore production). They also tested potential differences among three of the genetic lineages of the pathogen—NA1 (prevalent in U.S. forests), NA2 (found in some nurseries in Pacific coast states), and EU1 (found in nurseries and – since 2015 – in some wildland forests in Oregon). The team also studied the effect of temperature on infectibility. Their goal was to help focus regulations so they will be more effective.

The studies clearly show that the relationship between P. ramorum and various hosts is complex – both susceptibility and infectibility vary depending on the host species, pathogen genetic lineage, and environmental conditions, especially temperature. Results of testing of leaves for the presence of the pathogen were affected by such experimental choices as the concentration of zoospores, temperature, plant host, pathogen genotype, and by the interaction between host and pathogen genotype. Stem results were mostly affected by host and host-pathogen genotype interaction.

Hosts bearing the most severe infections do not always support the highest levels of sporulation, so they are not necessarily the most likely to spread the disease.

Regulators also cannot always generalize re: the pathogen’s impact on plant hosts based on the hosts’ taxonomic relationship. Results were fairly similar for congeneric species within the genera Rosa, Prunus, and Syringa, but quite different for species within the genera Ilex, Gaultheria, and Osmanthus.

It is clear that basing regulatory or best management practices on any one pathogen-host-environment relationship is likely to lead to failure, leaving our forests inadequately protected

The findings that pertain most directly to early detection of infections and those that otherwise promote spread of the pathogen are my focus here.

Hosts that Support Sporulation / Spread of Disease

At least five host species are much more infectious than Rhododendron catawbiense. Hosts that support the highest levels of sporulation were Syringa vulgaris, Hamamelis intermedia, and Syringa meyeri. Hosts that support medium-high levels of sporulation were Rosa gymnocarpa and Syringa pubescens subsp. patula.  

Two of the Syringa species support high levels of sporulation, but rank low on overall susceptibility. Rosa gymnocarpa ranked fourth for levels of sporulation, but only fifteenth for overall susceptibility. At least six other species join this group of taxa that are highly infectious without displaying noticeable symptoms. Note than none of these top disease drivers is included in the so-called “filthy five” genera which are the focus of federal and state detection efforts. These genera are Rhododendron spp., Camellia spp., Viburnum spp., Pieris spp., and Kalmia spp.

One of the “filthy five” is Rhododendron catawbiense. It is often used as a standard against which to compare other species’ vulnerability. R. catawbiense supports a somewhat lower level of sporulation than do the species listed in the preceding paragraph. Again, disease severity is not a reliable cue to the likelihood of supporting sporulation and disease spread. Thus, the Hamamelis intermedia was the only species that scored high for both sporulation and susceptibility.

Temperatures Affect Infection Rates

A temperature of 20°C [68o F] was found to be ideal for maximum sporulation by all three genotypes. However, the NA1 genotype was a relatively good sporulator at 12oC [53oF]. The NA2 genotype sporulates prolifically at 25°C [77oF], but produces fewer sporangia than the other two genotypes at 12oC. These findings suggest which genotype might pose a greater risk in warmer or cooler regions than those supporting the current wildland infestations in California and Oregon. Thus, if NA2 spreads via the nursery trade to warmer regions, such as the area of the Southeast identified by various risk maps developed in the past [See maps on pages 14 – 16 in chapter 5 of Fading forests III, available here], it might pose a higher risk. This discovery intensifies concern arising from the fact that many of the P. ramorum-infected plants shipped to Indiana – and presumably other eastern states – in 2019 were of the NA2 lineage. States that received infected plants in 2019 included Alabama, Arkansas, Kentucky, Missouri, North Carolina, Tennessee, Virginia, and West Virginia.

Considering individual host species, Gaultheria shallon, R. catawbiense, Osmathus delayayi and Hamamelis intermedia supported good sporulation at the higher temperatures whereas Laurus nobilis, Syringa vulgaris, and Magnolia stellata supported better sporulation in cooler climates. Note that H. intermedia and S. vulgaris support prolific sporulation; the latter is a “symptomless superspreader”.

Garbelotto et al. note that Magnolia stellata is both highly susceptible and highly infectious at 12°C and thus able to spread the infection in colder areas. This advice to limit use of this species in cooler areas runs counter to horticultural experts’ guidance to plant this shrub in USDA Hardiness Zones 4–9 – which include virtually all the lower 48 except the most northern parts of Montana, North Dakota, and Minnesota. Clearly, star magnolia is a popular plant in colder regions. At the other end of the spectrum, Gaultheria shallon, Hamamelis intermedia, and Mahonia aquifolia were both highly susceptible and infectious at 25 °C, thus their use should be limited in warmer areas. All three include warm regions in their native ranges. 

Early Detection

There are two ways to carry out early detection surveys.

(1) The first is detection of infection in plants themselves. Garbelotto et al. determined that 14 plant species are highly or moderately susceptible to infection even with relatively limited inoculum sources. Intense monitoring of these species would be likely to detect new infestations. Three of the highly susceptiblespecies, namely Syringa meyeri, Syringa pubescens subsp. patula and Hamamelis intermedia, are potentially more susceptible than R. catawbiense.

Hamamelis x intermedia ‘Angelly’ 01.JPG Wikimedia Commons

Based on the relative ease of pathogen re-isolation from the following host species after they had been inoculated at low levels, Syringa meyeri, Syringa pubescens subsp. patula, Hamamelis intermedia, Syringa vulgaris, Osmanthus delavayi, and Magnolia grandiflora indicated that a larger number of plants in the production facility had become infected.

(2) A second approach to early detection monitoring would be to focus on those host taxa able to support the most robust sporulation when infected by low levels of inoculum. This approach emphasizes curtailing spread.

As I noted above, Garbelotto et al. conclude that five species could spur significantly faster disease spread due to higher transmission rates coupled with higher susceptibility rates. These five species are Syringa vulgaris, S. meyeri, and S. pubescens subsp. patula; Hamamelis intermedia; and Rosa gymnocarpa. Note than none of these disease drivers is included in the so-called “filthy five” genera on which regulators focus now detection efforts.

Several species appeared less diseased, but supported more vigorous sporulation (e.g., Syringa vulgaris, S. pubescens subsp. patula and Rosa gymnocarpa). Others were more diseased but supported less sporulation (e.g., Prunus laurocerasus and Prunus lusitanica). Therefore, nursery managers and regulators should not rely on visual assessment of disease intensity to judge spread risk.

Other Information

Comparing the three genotypes, EU1 was most aggressive in terms of disease incidence at both low and high inoculum loads. At low levels of inoculum, NA1 lineage was comparable in terms of disease severity.

However, at higher inoculum loads NA1 was clearly the most infectious based on the number of sporangia produced on infected hosts. Garbelotto et al. conclude that the co-mingling of the EU1 and NA1 lineages in Oregon forests might result in a highly destructive forest disease, as both virulence and transmission potential would be maximized. There is the further risk that the presence of the two genetic lineages, which have different mating types, might enable sexual reproduction/ genetic exchange between the two lineages.

Sources

Matteo Garbelotto, M., D. Schmidt, T. Popenuck. 2020. Pathogenicity and infectivity of Phytophthora ramorum vary depending on host species, infected plant part, inoculum potential, pathogen genotype, and temperature. Plant Pathology 2020;00.1

Phytophthora ramorum – a deadly forest pathogen, surviving and spreading as three strains in North America. “Plant Pathology” Highlight. https://www.bspp.org.uk/phytophthora-ramorum-a-deadly-destructive-forest-pathogen-surviving-and-spreading-as-three-strains-in-north-america-on-more-than-100-ornamental-hosts-from-leaf-to-stem-across-a-range-of-t/

Posted by Faith Campbell

We welcome comments that supplement or correct factual information, suggest new approaches, or promote thoughtful consideration. We post comments that disagree with us — but not those we judge to be not civil or inflammatory.

For a detailed discussion of the policies and practices that have allowed these pests to enter and spread – and that do not promote effective restoration strategies – review the Fading Forests report at http://treeimprovement.utk.edu/FadingForests.htm

SOD marches on … & questions remain on the 2019 outbreak

dead tanoak killed by P. ramorum in Oregon;
photo courtesy of Oregon Department of Forestry

Stunning 2019 Nursery Outbreak – Continuing Story

I have blogged often about the sudden oak death pathogen Phytophthora ramorum. The most recent blogs have focused on last year’s episode in which infected plants were sent to retail nurseries in many states. Indeed, the 2019 outbreak led to the largest trace-forward investigation for the USDA APHIS’ Phytophthora ramorum program in a single year for more than a decade. A year later, much is still unclear. For example, based on reports last year, I told you that 18 states had received positive plants. APHIS now says it was 14.

In response to states’ requests, APHIS issued a “Hotwash Report” (described in the June 2020 newsletter of the California Oak Mortality Task Force (COMTF); see source list at the end of the blog for the url). The “Hotwash Report” says APHIS traced the infected plants back to two nurseries, but I have obtained information about efforts at only one – in Washington state – and even that information is not as explicit as I think should be. In the April COMTF newsletter, the Washington State Department of Agriculture reports only that compliance surveys at one wholesale shipping nursery would be more intense than usual. I believe the second nursery implicated in the event is in British Columbia, but the Canadian Food Inspection Agency has said it saw no evidence that a Canadian nursery had shipped infected plants to the U.S.

Indiana officials reported (Press et al.) that the infected plants received in that state were of the NA2 clonal lineage. This is the first report of the NA2 lineage outside British Columbia, Washington, and California and is thus especially significant. The outbreak caused Indiana authorities to ordered destruction of more than 6,100 rhododendron plants at retail outlets in Indiana. (April COMTF newsletter)

According to the June 2020 COMTF newsletter, APHIS revised its Phytophthora ramorum Domestic Regulatory Program Manual (available here). APHIS also reviewed the protocol governing responses to detection of P. ramorum in retail nurseries (available here).  The agency also plans to carry out a full program review but no timeline has been announced. 

It is not clear to me whether these actions satisfy the states or – most importantly – address the reasons why such a large breakout of nursery infestations escaped current regulatory safeguards.

APHIS Slow Walks a Revised Host List

Meanwhile, carrying out a promise made in May 2019 when APHIS revised the SOD regulations, APHIS has posted a revised list of officially recognized P. ramorum hosts (available here). Finally! The new list replaces one from 2013.

The new list recognizes only one new species (Gaultheria procumbens, eastern teaberry) as a proven host, based on completion of Koch’s postulates. (The scientific paper was published five years ago!) So far, APHIS would only recognize a host after Koch’s postulates were completed. But the agency has been unwilling to pay for the experimental work required.

That situation might be changing: APHIS says it is reviewing scientific publications and ongoing  research. The agency also invites scientists to contact the national program manager regarding plant taxa that they believe should be added to the regulated plant taxa list.

Meanwhile, we know that scientists have completed Koch’s postulates on several new hosts: Brisbane box, Lophostemon confertus, taken from samples of street trees dying in central Sausalito, Marin Co., California (COMTF June newsletter); and seven species of Arctostaphylos (manzanita) (COMTF April newsletter). So far, there’s no word from APHIS as to if or when it might act on these.

Nursery Situation in Individual States

California

Inspections under various federal and state regulatory requirements have detected infected plants in five nurseries (COMTF June newsletter).  Two are in counties with widespread infestations that ship only within the state. Infected plants were Camellia and Loropetalum (COMTF April newsletter). Three other nurseries, also that ship within the state, tested positive only in previous years. Trace investigations completed at four of these nurseries by June had detected no additional positive plants. (COMTF June newsletter)

Oregon

Western Oregon has a climate that favors P. ramorum. One result is intensification and spread of the forest infestation (see below); another is a perpetual problem with infected nurseries.

In fall 2019, Oregon Department of Agriculture detected positive plants and soil at an interstate shipper. The plants were destroyed. Trace-back detected no further positive detections. The areas with infested soil were taped off until authorities can carry out steaming to decontaminate (COMTF April newsletter).

Meanwhile, trace-back from a previously identified retail location led to a second commercial interstate shipper. Camellia, Pieris, and Rhododendron plants tested positive, along with three soil samples and one groundwater sample. This was the first detection for this wholesale location (COMTF April newsletter).

Then, a routine inspection detected P. ramorum at a third interstate shipper in early March 2020. As of April, seven Rhododendron plants tested positive. This was also the first detection at this particular nursery (COMTF April newsletter).

Meanwhile, the spring compliance surveys at 10 Oregon nurseries that ship interstate found no P. ramorum (COMTF October newsletter).

In August, Oregon Department of Agriculture conducted soil steaming at three nurseries that previously tested positive. The action was successful at two but not at the third due to irrigation issues. APHIS and ODA are working with the nursery to create an enhanced mitigation plan focusing on irrigation at the nursery (COMTF October newsletter).

However, trouble continues. In July, a North Carolina nursery reported positive Rhododendron plants that had been purchased from an Oregon nursery. Traceback detected infected Rhododendron plants at the site. Further tracebacks have been triggered at the locations where this material was purchased – apparently yet another nursery. The nursery is undergoing the final assessment to sign a federal compliance agreement and will be added to the list of nurseries sampled by ODA in fall (COMTF October newsletter).

Washington

Washington officials continue to detect P. ramorum in water bodies that have proved difficult to trace back to a plant source. Positive water samples were collected again from the pond at the botanic garden in Kitsap County – as has been true for most years since 2015.  Despite the continuing presence of the pathogen in the pond, authorities have not been able to find infected plants in recent years, including in 2020.

Authorities also detected a water-positive at a nursery participating in the P. ramorum compliance program. They have scheduled additional vegetation and water sampling (COMTF April newsletter). It is not stated whether this is the nursery apparently responsible for the 2019 spread event.

A third positive water sample was collected on a creek in Snohomish County. The state Department of Agriculture plans to follow up with two nurseries in the drainage. One had previously tested positive (COMTF April newsletter).

In June, the state conducted a trace-forward investigation on plants from a positive out-of-state nursery. Most plants had been sold at the retail level and were untraceable. However, 37 Rhododendron planted in several residential locations were sampled; six plants at four sites were positive. The Confirmed Residential Protocol has been enacted at all four locations (COMTF August 2020). Authorities also treated the soil at two of the planting sites (COMTF October newsletter).

The Risk of New Phytophthora Introductions Is Dire

The COMTF June newsletter summarizes the findings of studies by European forest pathologists. As I reported in an earlier blog, European researcher have identified more than100 previously unknown Phytophthora species through intensive surveys conducted during 2013 – 2019 in natural ecosystems of Japan, Taiwan, Vietnam, Indonesia, Chile, Nicaragua, Panama, Curacao, Egypt and eight European countries. Overall, 13,242 isolates were obtained, which could be assigned to 65 known and 101 previously unknown species. Two of the most damaging – P. cinnamomi and P. ramorum – are most likely native to Southeast Asia. The scientists recommend extensive host-range testing of forest tree and horticultural crop species to assess the potential threat posed by the import of living plants from Southeast Asia. Several presentations and factsheets with further information may be found here. https://www.ponteproject.eu/

Early in the year, I attempted to persuade APHIS to begin studies of possible hosts’ vulnerability, but I was told that APHIS does not do research. I also approached the Agriculture Research Service and USDA Forest Service. Perhaps academic scientist could obtain funding to carry out such studies through grants funded by the Plant Pest and Disease Management and Disaster Prevention Programs (under Section 7721 of the Plant Protection Act) or National Institute of Food and Agriculture.

Wildland Infestations – Threat to native plants; interactions with fire

The COMTF April 2020 newsletter reports the growing threat to manzanitas from P. ramorum. The genus Arctostaphylos includes more than 100 species of evergreen shrubs and small trees. Nearly half are classified as rare, threatened, or endangered. The center of diversity is in the San Francisco area – which overlaps with the area intensely infested by P. ramorum. At least 18 manzanita species support the pathogen. Koch’s postulates have been completed on seven of the most recently detected hosts, and are under way for two others. I am grateful to the California Department of Food and Agriculture for carrying out these studies; without them, APHIS would not recognize the plants’ host status. (Despite requiring completion of Koch’s postulates, APHIS does not fund these studies.)

A study of the interaction between P. ramorum and fire in California (October COMTF newsletter and Simler-Williamson et al.) found that frequently-burned forests were less likely to be invaded by the pathogen, had lower incidence of host infection, and lower occurrence and density of epidemiologically-significant hosts. The authors think that the fire-caused loss of tall, mature California bay laurel trees might temporarily dampen pathogen transmission and “release” susceptible species from significant inoculum pressure.

The June COMTF newsletter reports that the forest infestation in Oregon continues to spread. During spring 2020, Oregon detected 15 new P. ramorum infestations at or beyond the Oregon Generally Infested Area (GIA). The October newsletter reports that 38 stream drainages both inside and outside the SOD quarantine area were baited, and one at the northern boundary of the quarantine area was positive for P. ramorum. The Oregon Department of Forestry installed additional stream baits in the drainage to pinpoint the infestation, and plans a stream survey for the area. Planned eradication efforts have been impeded by funding cuts caused by Covid-19-related falls in tax receipts.

Posted by Faith Campbell

We welcome comments that supplement or correct factual information, suggest new approaches, or promote thoughtful consideration. We post comments that disagree with us — but not those we judge to be not civil or inflammatory.

For a detailed discussion of the policies and practices that have allowed these pests to enter and spread – and that do not promote effective restoration strategies – review the Fading Forests report at http://treeimprovement.utk.edu/FadingForests.htm

SOURCES

California Oak Mortality Task Force (COMTF newsletters) – archive of 2020 newsletters at https://www.suddenoakdeath.org/library/newsletter-archive/

Press, C.; Fieland, V.; Creswell, T.; Bonkowski, J.; Miles, L. and Grünwald, N.J. 2020 (First Look). First report of the NA2 clonal lineage of Phytophthora ramorum in Indiana. Plant Disease. https://doi.org/10.1094/PDIS-12-19-2543-PDN.

Simler-Williamson, A.B.; Metz, M.R.; Frangioso, K.M. and Rizzo, D.M. 2020. Wildfire alters the disturbance impacts of an emerging forest disease via changes to host occurrence and demographic structure. Journal of Ecology. Early View. https://doi.org/10.1111/1365-2745.13495

Pests Associated with Imports: Rising Risk for Gulf States

Port of Mobile, Alabama Photo by Port of Mobile Authority

In August and September I blogged about the rapid increase in volumes of imports from Asia, especially China, in 2020. At the time, the information available to me focused on the Pacific coast ports, especially Long Beach and Los Angeles.

In the earlier blogs, I mentioned three concerns:

1.  Had the collapse in trade and travel during spring 2020 so reduced user fees that Department of Homeland Security Bureau of Customs and Border Protection (CBP) had to furlough Agriculture Quarantine Inspectors?  AQI inspections provide important incentives for importers to follow U.S. and international rules to reduce the risk that pests will be present in imports, for example, in wood packaging. 

2. The list of imports from China in the first half of 2020 includes $1 billion worth of nursery stock. This is down about 7% from 2019. However, from the perspective of preventing plant diseases and pests, these imports continue to be high risk and are still not adequately addressed by U.S. policy.

3. Other Asian regions are gaining in import share. Thus we can expect to see more pests arriving from countries other than China, like Vietnam.  

Cutbacks in Numbers of Inspectors?

CBP staff have told me that they are shifting AQI inspectors from covering incoming passengers – which are still far fewer than before the Pandemic – to inspecting cargo. By doing so, CBP has avoided cutting back on the total number of inspections of imported goods and associated wood packaging.

This is fortunate since Congress has not passed a new Covid-19 financing bill that might have included an increase in the appropriation for DHS CBP. The Continuing Resolution currently in effect funds the government only until December 11. So we have another chance to ask for an increase in appropriated funds for CBP (and APHIS!) for the remainder of Fiscal Year 2021 (which ends on October 1, 2021).

Volumes of Imports from Asia – Especially China  

As I reported in the earlier blog, while U.S. imports from China declined significantly in 2019  and early 2020 compared to earlier years, by the summer imports had rebounded — more than doubled (by value) between March and July.

Shifts in U.S. Ports

According to the Journal of Commerce, there is a gradual shift away from the twin ports of Los Angeles and Long Beach in the proportion of imported goods entering the country.  LA-LB handled 37.7% of the loaded twenty-foot equivalent containers (TEUs) entering the United States in 2018. This fell to 33.5% in July 2020. The initial reason was a decrease in imports from East Asia (including China, Hong Kong, Japan, South Korea, and Taiwan) compared to Southeast Asia, Europe, then South America and, finally, South Asia (primarily India).

Other source regions – e.g., the Caribbean, Middle East, Pacific, Africa, and Atlantic – were all below 2% of total numbers of TEU in all three years, and changed minimally over this period.

Another reason for the shift in ports utilized by importers is congestion and delays at North American Pacific coast ports, especially Los Angeles-Long Beach. U.S. imports from Asia moving through LA-LB increased 22% in both September and August from the same months last year – 828,880 TEU in September after 832,210 TEU in August.

Congestion is also a problem at the Canadian ports of Vancouver and Prince Rupert – which have actually seen small decreases in numbers of incoming containers.

One result is a small but significant shift to Gulf Coast ports, which have become more accessible through the widening of the Panama Canal in 2016. Before the Canal was widened, these ports handled less than 3% of total US imports from Asia. In the first nine months of 2020, US Gulf ports handled 608,387 TEU from Asia – or 5.2% of total US imports from Asia. This was a 5% increase from the same period last year.

These ports, stretching from Houston to Tampa, benefit from easy and relatively cheap rail transport to inland U.S. and even Canadian cities. Another factor is the heavy presence of Walmart – which has major distribution centers in Mobile and Houston.

The Gulf coast ports are expected to expand their importance as gateways for Asian imports as ocean carriers add more capacity between the two regions and ports upgrade and expand. New Orleans and Houston plan major expansions. Port Tampa Bay notes its proximity to markets around the Southeast. Already, import volumes into Tampa during the first nine months of 2020 were nearly double the prior year’s level. Tampa hopes to double its capacity over the next five years.

U.S. imports from Asia in October were 22.6% higher than a year ago. Imports through the East and Gulf coast ports jumped 14.6% and 48.4% from September 2020. Houston and Baltimore saw the greatest increases since September. There were also shifts in Pacific ports. Still, the Los Angeles-Long Beach port complex handled 49% of total US imports from Asia in October 2020.

Pest Risks to the Gulf Coast from Southeast Asia

Rising volumes of imports into the Gulf Coast present new opportunities for non-native insects and pathogens. The warm, wet climate of the region might be far more suitable to some insects and pathogens from tropical and subtropical Asia than the dry climate of southern California (except for areas that are irrigated artificially, such as golf courses, parks, and plant nurseries!).

redbay grove killed by laurel wilt; Photo by Scott Cameron

Already, the redbay ambrosia beetle and its associated pathogenic fungus has decimated native redbay and swamp bay trees and now threatens sassafras (see write-up under the “invasive species” tab here.)

Another Southeast Asian ambrosia beetle – the polyphagous shot hole borer with its associated pathogenic fungus – might also find the Gulf Coast states more inviting than southern California. In California, it is causing the greatest damage to trees that are artificially irrigated. Numerous tree species native to or grown in the Gulf states are known hosts, e.g., box elder, sweetgum, and southern magnolia. (PSHB is described under the “invasive species” tab here.) Both ambrosia beetles apparently were introduced via wood packaging material.

Southeast Asia is also the place of origin of other pathogens which – in this case – would more probably be introduced on imported plants rather than wood. These include the numerous species of Phytophthora recently detected in Vietnam.

As this region receives more goods from Asia, and as those goods arrive more rapidly so more likely to arrive alive, it is imperative that all stakeholders increase their vigilance to detect new invaders. And that they join others pressing for improved policies aimed at preventing introductions.

Posted by Faith Campbell

We welcome comments that supplement or correct factual information, suggest new approaches, or promote thoughtful consideration. We post comments that disagree with us — but not those we judge to be not civil or inflammatory.

For a detailed discussion of the policies and practices that have allowed these pests to enter and spread – and that do not promote effective restoration strategies – review the Fading Forests report here.

Beech Leaf Disease – Inspect Trees for Symptoms! Help Determine the Extent of this Disease

Beech trees have leafed out – so now is the time to search for symptoms of beech leaf disease.

Since its first detection near Cleveland in 2012, BLD has now been detected in 40 counties in Ohio, New York, Pennsylvania, Connecticut, and Ontario.  (see map)

I ask your help now because homeowners detected the outbreaks in Connecticut in 2019. (It is often homeowners or curious citizens who detect outbreaks of tree-killing pests.)

What to look for – symptoms:

  • Dark bands between lateral veins of leaves. Banding is most apparent when viewing from below, looking upwards into the canopy. Banding is evident immediately upon leaf-out in the spring.
  • Aborted bud development and reduced leaf production.
  • Later stages result in heavily banded-darkened leaves that are thickened and leathery in texture, often with shriveled or curled edges.

All range of symptoms can be present on the same branch. Symptoms on individual leaves do not advance over the course of the summer. Severely affected leaves can drop off as summer progresses, sometimes as early as June. So the early season – now – is the best time to search.

Cleveland MetroParks has posted a pest alert (from last year), a report on symptom progression  with good photos, and instructions for participating in the Beech Tree Health Survey. Survey apps are available as iOS: https://apps.apple.com/us/app/tree-health-survey/id1498515762 or Android: https://play.google.com/store/apps/details?id=com.KentState.TreeHealth&hl=en_US

Go to https://www.clevelandmetroparks.com/parks/education/publications and scroll down to the Beech Leaf Disease section (it is in large font so you won’t miss it).

Where to look? See the map of the range of American beech.

Range of American beech; source Wikimedia

In addition to checking American beech (Fagus grandifolia), also examine European beech (F. sylvatica), and Oriental beech (F. orientalis).

I encourage you to use one of the apps. However, if you are not but see something suspicious, send me a picture by using the “contact us” button. I will take a quick look, consult with experts, and – if they see what appear to be symptoms – they will tell me and I will tell you how to contact plant health authorities in your state or province.

 Remember to include your email and phone number in your message to me – the “contact” form by itself does not provide sufficient information for me to respond to you.

Posted by Faith Campbell

We welcome comments that supplement or correct factual information, suggest new approaches, or promote thoughtful consideration. We post comments that disagree with us — but not those we judge to be not civil or inflammatory.

For a detailed discussion of the policies and practices that have allowed these pests to enter and spread – and that do not promote effective restoration strategies – review the Fading Forests report at http://treeimprovement.utk.edu/FadingForests.htm

SOD – questions that need answers

SOD in the nurseries

infected rhododendron
photo by Jennifer Parke
Oregon State University

As you may remember, in May 2019, we became aware of a troubling outbreak of the sudden oak death pathogen Phytophtora ramorum in the nursery trade. The discovery was made by Indiana authorities, who carefully inspected plants being sold in the state.

Briefly, 28 states initially learned that they might have received plants from the suspect sources. Later, APHIS determined that plants exposed to the pathogen had been sent to 18 states – Alabama, Arkansas, Iowa, Illinois, Indiana, Kansas, Kentucky, Michigan, Missouri, Nebraska, North Carolina, Ohio, Oklahoma, Pennsylvania, Tennessee, Texas, Virginia, and West Virginia. Of these, seven (Iowa, Illinois. Indiana, Kansas, Missouri, Nebraska, Oklahoma) plus Washington were known to have received P. ramorum-positive nursery stock. [California Oak Mortality Task Force Newsletter August 2019]

The 2019 episode was just the latest of several occasions since 2004 in which infected plants have been widely distributed by the nursery trade, despite federal and state regulations.

APHIS delays in explaining the situation and what actions it was taking led the states to complain through a letter from the National Plant Board.

For discussions of the 2019 espisode, see my earlier blog or the California Oak Mortality Task Force newsletter for February 2020.

What have we learned from this episode?

1) Three West coast states – California, Oregon, and Washington – are a usual source for the nursery trade of plant taxa that happen to host the P. ramorum pathogen plants. These states’ climates are conducive to growth of these plants and of the pathogen. After repeated nursery outbreaks over 16 years, I think it is time to question continued reliance on such a high-risk source for these plants.

2) APHIS funds the federally-mandated inspection programs in the three states through the “specialty crops” line of the agency’s annual appropriations. Funding levels have apparently remained steady in recent years (COMTF Feb 2020), despite increases in the overall funding for the “specialty crops” line in recent years. I – and some of you! – have lobbied for these increases precisely in order to address the P. ramorum threat. Why has the funding not been increased?

3) While APHIS allocated $352,945 (COMTF February 2020) from the Plant Pest and Disease Management and Disaster Prevention program to help states carry out nursery surveys in 14 states following the 2019 incident, some of the affected states were not included in the program and some states that had not received suspect plants were. States that did not get funding in Fiscal Year 2020 (2020 award report) included three where P. ramorum-positive plants were detected: Iowa, Illinois, and Indiana; and one state that had a scare – Pennsylvania received plants but none tested positive. Seven states received P. ramorum survey funds through the Plant Pest and Disease Management and Disaster Prevention program although they had not received positive plants in the 2019 incident. These were Maryland, Massachusetts, Nevada, New York, North Dakota, Rhode Island, and South Carolina.

The Plant Pest and Disease Management and Disaster Prevention program distributes $70 million annually, and is not subject to annual appropriations. Does a national crisis play any role in determining which projects get funded? Or are decisions made entirely on a proposal by proposal basis and so depend on states’ priorities and individuals’ grant-writing skills?

4) Even now, on the verge of a new plant shipping season (if one occurs given the Covid-19 virus shutdowns), I have seen no public information clarifying how the inspection systems in Washington, British Columbia, and at the U.S. border failed to detect the infested plants before they were shipped. Trace-back efforts carried out by state and U.S. authorities pointed to a nursery in British Columbia as the original source of the infested plants. However, the Canadian Food Inspection Service (CFIA) determined that no Canadian nursery shipped infected plants to the U.S. in 2018 or 2019. See the next paragraph for a description of APHIS’ efforts to resolve this discrepancy.

According to information in the Oregon Department of Agriculture report for 2019, plant imports from Canada are inspected by DHS Customs and Border Protection (CBP) agriculture specialists, not by APHIS. Apparently, CBP has been relying on rules applicable to fruits and vegetables (Q-56) rather than the more stringent provisions of the plants for planting regulation (Q-37). Alerted by Oregon to the importation of 15 Euonymus plants infested by a federally-designated quarantine pest (a thrips), the National Plant Board sent a letter to APHIS in August 2019 asking that it correct CBP’s inspection process.

In March 2020, APHIS sent a letter to the states saying it had amended its Manual and guidance to CBP agricultural inspectors to clarify that all plants for planting must be handled in accordance with the more stringent Q-37 regulations. Furthermore, APHIS is working with CFIA to clarify understanding of each other’s P. ramorum procedures. The letter states that APHIS might consider prohibiting importation of P. ramorum hosts from Canada until CFIA demonstrates that it has adopted effective management measures.

This action by APHIS demonstrates a new seriousness in addressing P. ramorum. I hope this gravitas will persist and carry through to 1) strengthening theregulatory conditions governing domestic production and sales see following section); 2) providing financial and other support to the states (see above about the “specialty crops” appropriation); 3) funding additional studies to clarify the host list and modes of transmission; and 4) using its authority under NAPPRA to curtail imports of plants from Vietnam and other areas where there are large numbers of newly detected Phytophthora species that might threaten North American plant species.  

infested plants detected by Indiana inspectors

I question sufficiency of inspection and mitigation regime

(as described in the February 2020 COMTF newsletter)

When alerted to the infected plants turning up in Indiana, in May 2019, Washington State Department of Agriculture (WSDA) began trace-back investigations. The large wholesale shipping nursery that supplied the plants appears to have acted quite responsibly – it destroy 54,000 plants, cooperated in the Critical Control Point assessment, and implemented mitigation actions. However, I am disturbed to read that the destruction of plants in the 10-meter quarantine radius from plants detected to be infected was a voluntary action. Why don’t the regulations require destruction of nearby hosts?

Descriptions of the western states’ inspection systems – those tied to this specific nursery episode and routine inspections under federal and state P. ramorum programs – indicate to me that P. ramorum is circulating in nurseries in the west coast states, but is evading detection. I cite examples from all three states.

One of the positive nurseries in California in 2019 had been found to be positive in previous years and is considered to be in compliance with quarantine regulations. Yet these measures have not been sufficient to ensure that the nursery is pathogen-free now – as illustrated by its testing positive in 2019.

In Oregon, a retail nursery found to have infected plants destroyed all host material located in the block. Is this action sufficient to ensure that the nursery is now pathogen free? What about the soil, water, cull piles, etc.?  Oregon trace-back surveys led to various suppliers that had previously not been known to be infested. This leads me to think that the pathogen is circulating below regulators’ attention.

In the wake of the 2019 crisis, Washington State Department of Agriculture (WSSA) inspected “opt-out” nurseries – those that had decided not to join APHIS’ program to ship interstate, but continued to ship within the state. WSDA relied on visual inspection only of host material; the agency collected no samples from plants or nursery soils, water, or plant waste (Feb 2020 COMTF). Given all we know about the difficulty of detecting P. ramorum, I think we need more intense inspections that do sample soils, water, and any nearby plant waste (cull piles).

Meaning of Stream Detections?

The P. ramorum pathogen continues to turn up regularly in water bodies. At a botanical garden in Washington State, plant samples have been negative since February 2016. However, water baits from a small pond were positive in 2019 and previous years. Washington’s Sammamish Riverhas been positive since 2007. In the Southeast, seven streams tested positive in 2019. Most if not all have been positive consistently or at least repeatedly for years. All these positive streams are associated with nurseries previously positive for the pathogen. However, plants in the vicinities of these streams show no symptoms.

The same is true in Vietnam: P. ramorum was found in seven out of eight high-elevation streams sampled, but none of the plants belonging to families that have proved highly vulnerable in North America and Europe had any disease symptoms (Jung et al, 2020. A Survey in Natural Forest Ecosystems of Vietnam Reveals High Diversity of both New and Described Phytophthora Taxa including P. ramorum. Forests, 2020, 11). The Jung et al. 2020 findings are discussed in the COMTF Feb. 2020 newsletter and my recent blog.

SOD in the woods

dead coast live oak in California
Joseph O’Brien, USFS

The COMTF February 2020 newsletter summarizes the worrying increase in disease in California woodlands in recent years, which followed the record wet spring of 2017. Aerial surveys documented a big increase in dead tanoak trees and affected acreages in 2018, followed by a smaller increase in 2019 – although still much higher than in 2017. [Details: in 2017, 21,000 dead trees were mapped across 18,000 acres; in 2018, 1.6 million dead trees across 106,000 acres; in 2019, 885,000 dead trees across 92,000 acres.]

California officially records as infested only those counties where infestations have been confirmed by California Department of Food and Agriculture or county Agricultural Commissioners. California currently lists 15 counties as infested. Recent observations by academics or other non-officials of Phytophthora ramorum in Del Norte and San Luis Obispo counties have not yet been confirmed by officials so neither is included in the official quarantine. I understand the need to be certain about reported detections, but we should remember that the disease is probably more widespread than official data indicate.

The newsletter reports Oregon’s treatment efforts – which have totaled 7,300 acres since 2001. I am pleased that Oregon Department of Forestry now has an Environmental Quality Incentives Program (EQIP) project with the USDA Natural Resources Conservation Service and that both the Bureau of Land Management and USDA Forest Service are treating infected areas.

treatment of SOD-infested site
in Oregon
USFS

Still, the quarantine area now covers 31% of Curry County, the EU1 lineage is established in the forest, and ODF and its partners lack sufficient resources to treat all infected areas.

Washington State doesn’t have (known) forest infestations, but it continues to find the pathogen in water bodies; the Sammamish River in King County has been positive since 2007.

In the East, seven states (Alabama, Florida, Georgia, Mississippi, North Carolina, South Carolina, and Texas) participated in the USFS Cooperative Sudden Oak Death Early Detection Stream Survey in 2019. A total of 48 streams were surveyed. P. ramorum was detected from seven streams – five in Alabama, one in Mississippi, and one in North Carolina. All positive streams were associated with nurseries previously positive for the pathogen.

Finally, the newsletter summarizes an article providing advice on managing SOD’s impacts – specifically, conservation of tanoak.

SOURCES

February 2020 issue of the California Oak Mortality Task Force newsletter http://www.suddenoakdeath.org/wp-content/uploads/2020/02/COMTF-Report-February.pdf

Oregon Department of Agriculture Plant Protection and Conservation 2019 annual report

Posted by Faith Campbell

We welcome comments that supplement or correct factual information, suggest new approaches, or promote thoughtful consideration. We post comments that disagree with us — but not those we judge to be not civil or inflammatory.

Growing Pathogen Threat from Southeast Asia – US Unprotected

APHIS can protect our native & agricultural plants – but will it?

Imports of large numbers of plants for planting from Southeast Asia represents a significant biosecurity risk for forestry, horticulture, and natural ecosystems in North America and Europe.  This threat is likely to grow unless APHIS takes action under its emergency authorities.

Recent pest introductions and related studies indicate that Southeast Asia is a newly-discovered center of origin for plant pathogens. Places of particular concern are Vietnam, southern Yunnan Province and Hainan Island of China, northern Laos, the eastern Himalayas, and Taiwan. Significant pathogens and associated insects apparently centered in these areas include the sudden oak death pathogen (Phytophthora ramorum) and other Phytophthora species; and several ambrosia beetles and associated fungi, including the laurel wilt fungus (Raffaelea lauricola) and its primary vector (Xyleborus glabratus), and the polyphagous (Euwallacea whitfordiaodendrus) and Kuroshio shot hole borers (Euwallacea kuroshio).

Southeast Asia is attractive to the plant trade because of the region’s high floral diversity, including such sought-after families as Ericaceae (rhododendrons). Indochina has more than 10,350 vascular plant species in 2,256 genera – equaling more than 20% of the world’s plant species (Jung et al. 2019).

Pathogens are notoriously difficult to detect during inspections at the time of shipment. One-time inspections of high volume imports are especially weak and prone to failure.

How do we protect America’s flora?

APHIS could — but has not yet — developed requirements that these countries institute integrated pest management procedures for their exporting nurseries – as provided under amendments to APHIS’ Q-37 regulation and ISPM#36. In any case, it is unlikely that such procedures would minimize the risk because many of the plants that would be imported would probably be wild-collected.

APHIS has – and should use – far more effective means to minimize risk. These are the Federal orders and listing process known as “not authorized for importation pending pest risk assessment” or NAPPRA. If – despite the scientific evidence – APHIS continues to allow high volumes of dangerous imports, the agency should immediately institute new phytosanitary controls to its inspection process. These include relying on risk-based inspection regimes and molecular high-through-put detection tools.

Supporting Material

SOD-killed tanoaks in Big Sur; photo provided by Matteo Garbelotto, UC Berkeley

Phytophthora species

A team of European pathologists, led by Thomas Jung and including Clive Brasier and Joan Webber (see full citation at the end of this blog) surveyed Phytophthora species by sampling rhizosphere soils in 25 natural and semi-natural forest stands, isolations from naturally fallen leaves, and waters in 16 rivers in temperate and subtropical montane and lowland regions of Vietnam during 2016 and 2017.

These studies detected 13 described Phytophthora species, five informally designated taxa, and 21 previously unknown taxa. Detections were made from soil samples taken from 84% of the forest stands and from all rivers.

As I reported in am earlier blog, P. ramorum and P. cinnamomi were among those species detected. Both the A1 and A2 mating types of both P. ramorum and P. cinnamomi co-occurred.

The survey also detected at least 15 species in other genera of oomycetes.

The scientists conclude that most of the 35 forest Phytophthora species detected are native to Vietnam or nearby surrounding areas, attributing species in Phytophthora clades (taxonomically related groups) 2, 5, 6, 7, 8, 9, and 10 as native to Indochina. Different clades were detected in high-elevation vs. lowland rivers, cooler (subtropical) vs. tropical streams, and in soils vs. streams. Given the relatively limited number and diversity of the sampled sites and ecosystem types, it is likely that the true Phytophthora diversity of Vietnam is markedly higher (Jung et al. 2019)  

Worrying diversity of Phytophthora has been detected in other areas of Southeast Asia. A 2013 survey in natural forests and streams of Taiwan detected 10 described species and 17 previously unknown taxa of which 9 were of hybrid origin. In three areas in northern Yunnan, a Chinese province adjacent to northern Vietnam, eight Phytophthora species were isolated from streams running through sclerophyllous oak forests; two were recovered from forest soil samples. In montane forests of the tropical island Hainan, located in the South China Sea close to Vietnam, six Phytophthora species were found (Jung et al. 2019).

These studies are being conducted in the context of scientists discovering numerous new species of Phytophthora in recent decades. Since 1999, the number of described species and informally designated taxa of Phytophthora has tripled. World-renowned experts Clive Brasier anticipates that between 200 and 600 species of Phytophthora are extant in natural ecosystems around the world (Jung et al. 2019).

In the Vietnam survey, P. ramorum was the most widespread species. While genetic studies indicate ancestral connections to the four P. ramorum lineages (genetic strains) introduced to North America or Europe, further studies are under way to clarify these relationships (Jung et al. 2019).

Jung and colleagues found P. cinnamomi to be the most common soilborne Phytophthora species at elevations above 700 m. Two genotypes of the P. cinnamomi A2 mating type are causing epidemics in numerous natural and managed ecosystems worldwide. There was some evidence that the more frost sensitive A2 mating type might be spreading into higher altitudes in Vietnam (Jung et al. 2019).

Most of the Phytophthora species detected in the rhizosphere were not associated with obvious disease symptoms. (The principal exception was the A2 mating type of P. cinnamomi in montane forests in northern Vietnam.) (Jung et al. 2019) This lack of disease greatly reduces the chances of detecting the oomycetes associated with any plants exported from the region – there are no symptoms.

Since southern Yunnan, northern Laos, and the eastern Himalayas belong to the same biogeographic area those areas might also harbor endemic P. ramorum populations. Further surveys are needed to confirm this hypothesis (Jung et al. 2019).

Phytophthora lateralis – causal agent of Port-Orford cedar root rot – also probably originated in the area, specifically Taiwan (Vettraino et al. 2017).

Implications for phytosanitary measures

Many of the native Asian forest Phytophthora species have co-evolved with a variety of tree genera also present in Europe and North America, including Fagaceae, Lauraceae, Aceraceae, Oleaceae, and Pinaceae. Numerous examples demonstrate a strong potential that trees in these families that have not previously been exposed to these Phytophthora species might be highly susceptible. Scientists have begun an extensive host range study of Phytophthora species from Asia and South and Central America. One part of this study found that five Asian Phytophthora species caused significant rot and loss of fine roots and lateral roots in three European species of chestnut and oak (Jung et al. 2019).

Other pathogens

Studies by separate groups of scientists have concluded that several beetle-fungus disease complexes are native to this same region.

Sassafras – photo by David Moynihan

Both the laurel wilt fungus Raffaelea lauricola and its primary vector Xyleborus glabratus probably originated in Southeast Asia; there are probably different strains or genetic makeups across their wide ranges. For example, Dreaden et al. 2019 found that the fungus population from Myanmar differed genetically from those found in Japan, Taiwan, and the United States. Others had already expressed concern about the possibility that new strains of R. lauricola might be introduced (Wuest et al. 2017, cited in Cognato et al. 2019).

Cognato et al. 2019 found that the beetle occurs in deciduous forests from southern Japan to Northeast India, so genetic variation across this range is likely. In fact, they have separated the species X. glabratus into three species. They found that some of the beetles might thrive at 40o North – the latitude of central Illinois, Indiana, and Ohio and southern Pennsylvania. The ability of the vector of laurel wilt disease to spread so far north poses an alarming threat to sassafras (Sassafras albidum) – which is a major understory tree in forests of these regions.

It is unknown whether these new species and X. glabratus lineages are associated with different fungal strains. In company with the pathologists cited above, Cognato et al. 2019 warn that preventing introduction of the three beetle species to other regions is prudent. Cognato et al. 2019 point out that if other beetle lineages from the southern extent of their range can tolerate hotter and drier conditions, they might pose a greater risk to host species in the more arid areas of California and Mexico. In addition, Central America is at great risk because of the numerous plant species in the vulnerable Lauraceae found there.

Also from the region are two beetle-fungus combinations killing trees in at least seven botanical families, including maples, oaks, and willows, in southern California. The polyphagous shot hole borer (Euwallacea whitfordiaodendrus) apparently is native to Vietnam (Eskalen et al. 2013) and the closely related Kuroshio shot hole borer (Euwallacea kuroshio) to Japan, Indonesia, and Taiwan (Gomez et al. 2018).  

What you can do

Getting APHIS to act

1) communicate concern about the risk to APHIS leadership and ask that the agency take action under its NAPPRA authority

2) communicate the same to intermediaries who can influence APHIS:

  • State phytosanitary agency – especially through regional plant boards and National Plant Board
  • Your Congressional representative and senators (especially if one or more serves on Agriculture or Appropriations committee)
  • Professional societies – American Phytophathological Society, Mycological Society, American Society of Entomologists, Society of American Foresters …

3) communicate the same to university leadership and ask that their lobbyists advocate to USDA

4) communicate the same to the media

2) Research on extent of North American tree species’ vulnerability to the Oomycetes and other associated microorganisms

Jung et al. 2019 say that studies are under way to identify potential pest-host relationships with important tree species. However, all the authors are Europeans. Is anyone carrying out tests on North American trees in the apparently most vulnerable families — Fagaceae, Lauraceae, Aceraceae, Oleaceae, and Pinaceae?

1) Communicate with colleagues, scientific societies, APHIS, Agriculture Research Service, National Institute of Food and Agriculture, and USFS to determine whether such tests are under way or planned.

2) In those cases where no studies are planned, work with above to initiate them.

Sources

Cognato, A.I., SM. Smith, Y. Li, T.H. Pham, and J. Hulcr. 2019. Genetic Variability Among Xyleborus glabratus Populations Native to Southeast Asia (Coleoptera: Curculionidae: Scolytinae: Xyleborini) and the Description of Two Related Species. Journal of Economic Entomology XX(XX), 2091, 1 – 11.

Dreaden, T.J., M.A. Hughes, R.C. Ploetz, A. Black and J.A. Smith. 2019. Genetic Analyses of the Laurel wilt Pathogen, Raffaelea lauricola, in Asia Provide Clues on the Source of the Clone that is Responsible for the Current USA Epidemic. Forests 2019, 10, 37

Eskalen, A., Stouthamer, R. Lynch, S.C., Twizeyimana, M., Gonzalez, A., and Thibault, T. 2013. Host range of Fusarium dieback and its ambrosia beetle (Coleoptera Scolytinae) vector in southern California. Plant Disease 97938-951.

Gomez, D.F., J. Skelton, M.S. Steininger, R. Stouthamer, P. Rugman-Jones, W. Sittichaya, R.J. Rabaglia, and J. Hulcr1/ 2018. Species Delineation Within the Euwallacea fornicatus (Coleoptera: Curculionidae) Complex Revealed by Morphometric and Phylogenetic Analyses. Insect Systematics and Diversity, (2018) 2(6): 2; 1–11

Jung, T., B. Scanu, C.M. Brasier, J. Webber, I. Milenkovic, T. Corcobado, M. Tomšovský, M. Pánek, J. Bakonyi, C. Maia, A. Baccová, M. Raco, H. Rees, A. Pérez-Sierra & M. Horta Jung. 2020. A Survey in Natural Forest Ecosystems of Vietnam Reveals High Diversity of both New and Described Phytophthora Taxa including P. ramorum. Forests, 2020, 11, 93   https://gcc02.safelinks.protection.outlook.com/?url=https%3A%2F%2Fwww.mdpi.com%2F1999-4907%2F11%2F1%2F93%2Fpdf&data=02%7C01%7C%7Cfcd843919a3348a4a56108d7974039ab%7Ced5b36e701ee4ebc867ee03cfa0d4697%7C0%7C1%7C637144174418121741&sdata=WayrZsxp3P9Kj0h1aDPZnzu4yjDGA2ZEuH9NZITFQF4%3D&reserved=

Vettraino,  A.M., C.M. Brasier, J.F. Webber, E.M. Hansen, S. Green, C.Robin, A. Tomassini, N. Bruni, A. Vannini. 2017. Contrasting microsatellite diversity in the evolutionary lineages of Phytophthora lateralis. Fungal Biology Vol. 121, Issue 2, February 2017, pp. 112-126

Posted by Faith Campbell

We welcome comments that supplement or correct factual information, suggest new approaches, or promote thoughtful consideration. We post comments that disagree with us — but not those we judge to be not civil or inflammatory.

Last Chance! to comment on proposal to restrict imports of certain plant taxa

rust on `ohi`a; photo by J.B Friday, University of Hawaii

As I blogged in December, APHIS is seeking input on a proposal to place several plant taxa in the category “not authorized pending pest risk analysis” (NAPPRA). The purpose of this proposed listing is to prevent introduction of plant pests or probable invasive plant species.

I urge you to comment before the deadline – this Friday, January 24.

In comments prepared for the Center for Invasive species Prevention (CISP), I applauded APHIS’ continued reliance on this authority to improve phytosanitary protections for our natural and agricultural resources. I noted, however, several weaknesses in the proposal – including several pathogens that I think should have been included, but were not. I summarize these comments here. 

1) There have been lengthy delays in proposing and finalizing lists of species to be regulated under this authority. While I strongly support listing of all plants in the family Myrtaceae that are destined for Hawai`i in order to reduce the risk that additional strains of the `ohi`a rust pathogen Austropuccinia psidii might be introduced and prove more damaging to native Hawaiian vegetation than the strain already present on the islands. However, this proposal comes 15 years after the pathogen was detected in Hawai`i and six years after publication of scientific documentation of the existence of more damaging strains of the pathogen.

2) When lists have been presented, they failed to include all appropriate species.

I am disturbed that APHIS did not include in the NAPPRA proposal Ceratocystis lukuohia and Ceratocystis huliohia, two pathogens that are killing millions of ‘ōhi‘a trees in Hawai`i under the name “rapid ‘ōhi‘a death”.

3) APHIS must act under other regulatory provisions to close some of the gaps left by this proposal.

The listing of plants in the Myrtaceae (see number 1 above) under NAPPRA does nothing to halt imports of cut flowers and foliage, which are widely recognized to be the pathway by which the rust was introduced to Hawai`i.  APHIS notes that is should act under other regulatory authority to close this pathway; I hope you will urge APHIS to take such action quickly, preferably initially by issuing a Federal Order.

4) APHIS has proposed 26 plant taxa for inclusion in the NAPPRA category because they might themselves be invasive. These proposals are generally well supported and deserve your support. Several plant taxa appear to pose significant ecological threats: two taxa of mangroves (Bruguiera gymnorhiza and Lumnitzera racemose); a vine that grows in Asian and Indian Ocean mangrove forests, Derris trifoliate; and several aquatic plants (Crassula helmsii, Elatine ambigua, Luziola subintegra, Philydrum lanuginosum, Stratiotes aloides); and Ligustrum robustum.

Remember that at least 50 species of aquatic plants are already considered invasive in the United States. At least eight species of Ligustrum are also invasive.

Update: Listing finalized

On June 2, 2021 APHIS finalized the NAPPRA listing originally proposed in November 2019.

The agency added to the category 26 plant taxa because they are invasive; all plants in the Myrtaceae family when destined to Hawai`i, and 43 other plant taxa that are hosts of 17 quarantine pests. 

The only change from the proposed action was to drop listing of the subfamily Bambusoideae because it is already regulated under NAPPRA to prevent introduction of other quarantine pests.

APHIS had received 132 comments from producers, importers, industry groups, conservationists, scientists, plant pathologists, ecologists, administrators, teachers, students, and private citizens. Most reportedly supported the proposed listing of Myrtaceae destined for Hawai`i and expressed no concerns about the proposed listing of most other taxa. I have blogged previously about the threat to Hawaii’s unique flora posed by the pathogen Australopuccinia psidii (the subject of this NAPPRA listing) and other non-native organisms – here and here.

A complete list of taxa listed under NAPPRA and the resulting restrictions on importation is posted at https://www.aphis.usda.gov/aphis/ourfocus/planthealth/import-information/permits/plants-and-plant-products-permits/plants-for-planting/ct_nappra  

Posted by Faith Campbell

We welcome comments that supplement or correct factual information, suggest new approaches, or promote thoughtful consideration. We post comments that disagree with us — but not those we judge to be not civil or inflammatory.

For a detailed discussion of the policies and practices that have allowed these pests to enter and spread – and that do not promote effective restoration strategies – review the Fading Forests report at http://treeimprovement.utk.edu/FadingForests.htm

Sudden Oak Death – Bad News All Around

SOD in California;
photo by Joseph O’Brien. courtesy of Bugwood

We know that the international trade in living plants is a major pathway by which tree-killing pathogens are being spread – some of them again and again. According to Grünwald et al. (2019), Phytophthora ramorum, the pathogen that causes Sudden Oak Death (SOD), has been introduced to North America and Europe – probably from Asia – at least five times. One lineage or genetic strain – EU1 – has been established on both continents (strains explained here). There is strong evidence of two separate introductions to Oregon, at least 12 to California.

Jung et al. 2015 state definitively that the international movement of infested nursery stock and planting of reforestation stock from infested nurseries have been the main pathway of introduction and establishment of Phytophthora species in European forests.  

Clive Btasier in Vietnam
photo from UK Forest Research

Jung et al. 2020 have demonstrated that P. ramorum probably originated in Vietnam.  This region appears to be a center of diversity for Phytophtoras and other Oomycetes: baiting of soil and streams resulted in the detection of 13 described species, five informally designated taxa, and 21 previously unknown taxa of Phytophthoras plus at least 15 species in other genera. Noting the risk associated with any trade in plants from this region, the authors re-iterated past appeals that the international phytosanitary system replace the “outdated and scientifically flawed species-by-species regulation approach based on random visual inspections for symptoms of described pests and pathogens” by instituting “a sophisticated pathway regulation approach using pathway risk analyses, risk-based inspection regimes and molecular high-throughput detection tools.”

Pathogen’s Spread Proves U.S. Domestic Regulations Governing Nursery Trade Are Inadequate

Last year I blogged about the most recent spread of Phytophthora ramorum through the nursery trade.  As of now, we know that shipments of potentially infected plants had been sent to 18 states. Infected stock had been detected in nurseries in seven of these (Iowa, Illinois, Indiana, Kansas, Missouri, Nebraska, Oklahoma) plus the source state, Washington [COMTF Newsletter August 2019].

Since then, I learned [COMTF newsletter for December 2019]   that these plants were infected by the NA2 strain of the pathogen. This is the first time that this strain has been shipped to states outside the West Coast. It is unclear what the impact will be if – as is likely – infested plants are still extant in purchasers’ yards. Both the NA1 strain (the strain established in most infested forests of California and Oregon) and the NA2 strain belong primarily to the A2 mating type, so the potential spread of NA2 lineages might not exacerbate the probability of sexual reproduction of the pathogen.

I applaud agencies’ funding of genetic studies to determine the lineage of the pathogen involved. It not only helps narrow the possible sources of infected plants, but also could be important in determining risk and management options.

I have long criticized USDA’s P. ramorum regulatory program – see Fading Forests III and my blogs discussing the most recent revisions to the regulations here and here. I believe that both the earlier regulations and the revisions finalized last May provide inadequate protection for America’s forests. 

The updated regulations do take a couple of important positive steps. First, APHIS is now authorized to sample water, soil, pots, etc. – and to act when it finds evidence of the pathogen’s presence. APHIS also now mandated nurseries found to be infested to carry out a “critical control point analysis” to determine practices which facilitated establishment and persistence of P. ramorum.

However, these improvements are severely undermined by continuing the five-year-old practice of limiting close scrutiny to only those nurseries that tested positive for the pathogen in the recent past. The flaw in this approach was starkly demonstrated by the pathogen’s spread in 2019. The Washington State nursery that was the source of the infected plants had not previously been positive, so it was under routine nursery regulation, not the more stringent federal P. ramorum program.

Too often various iterations of the regulations have allowed infected plants to be shipped. Between 2003 and 2011, a total of 464 nurseries located in 27 states tested positive for the pathogen, the majority as a result of shipments traced from infested wholesalers (Campbell). The number of nurseries found to have infected plants has since declined, but not dropped to zero. These include 34 nurseries in 2010 (COMTF February 2011 newsletter), 21 in 2012, and 17 in 2013 (Pfister). During 2014, state inspectors detected the SOD pathogen in 19 nurseries – 11 in the three west-coast states and eight in other parts of the country (Maine-1, New York-2, Texas-1, and Virginia-4) COMTF newsletter December 2014). Despite the continuing presence of the pathogen in the nursery trade, APHIS formalized existing practices that narrowed the regulators’ focus to only those nurseries with a history of pathogen presence. This approach has been shown to fail – we need APHIS and the states to find a way to broaden their scrutiny.

The most immediate impact of the continuing presence of P. ramorum in the nursery trade is the burden borne by eastern states’ departments of agriculture. They are obligated to seek out in-state nurseries that might have received infected plants; inspect those plants; and destroy the infected plants, test nearby plants, and try to find and retrieve plants that had been sold. The heaviest, and most direct, burden is borne by the receiving nurseries. Anger about bearing this burden for 15 years doubtless prompted the National Plant Board to adopt a tart resolution calling on APHIS to carry out a review of its communications to the states during the 2019 incident. The NPB also questioned whether current program processes and guidance are effective in preventing spread of this pathogen. 

Unfortunately, the NPB had not commented formally on the rule change when it was proposed.

The states’ frustration is exacerbated by the fact that under the Plant Protection Act, when APHIS takes a regulatory action it prevents states from adopting more stringent regulations. While the law allows for exceptions if the state can demonstrate a special need, none of the five applications for an exemption pertaining to P. ramorum was approved (Porter and Robertson 2011). I have been unable to find evidence of petitions submitted in the nine years since 2011.

In Case You Needed A Reminder: P. ramorum is a Dangerous Pathogen – as Proved by the Situation in the West states and Abroad

Continuing Intensification of the Already Bad Infestations in the West

tanoak mortality in Big Sur
photo courtesy of Matteo Garbelotto, UC Berkeley

As of 2014 (see COMTF November 2018 newsletter available here), perhaps 50 million trees had been killed by P. ramorum in California and Oregon. The vast majority were tanoaks (Notholithocarpus densiflorus)  – an ecologically important tree. 

Since 2014, the disease has intensified and spread in response to recent wet winters. In 2016 (see COMTF

November 2016 newsletter here) disease was detected for the first time in a fifteenth California county and new outbreaks or more severe infestations were recorded in seven other counties.  In 2019, SOD was detected in the sixteenth county. Tanoak mortality in California increased by more than 1.6 million trees across 106,000 acres in 2018.

Perhaps more disturbing, the disease has also intensified on the eastern side of San Francisco Bay – an area thought to be less vulnerable because it is drier and where there are fewer of the principal sporulation host, California bay laurel (see COMTF March 2017 newsletter here).

A second disturbing event is the detection in Oregon forests of the EU1 strain of Phytophthora ramorum. The August 2015 detection was the first instance of this strain being detected in a forest in North America. Oregon authorities prioritized removing EU1-infected trees and treating (burning) the immediate area, which had expanded to more than 355 acres – all within the quarantine area in Curry County. The legislature provided $2.3 million for SOD treatments for 2017-2019 (Presentation by Chris Benemann of Oregon Department of Agriculture to the Continental Dialogue on Non-Native Forest Insects and Diseases; reported here).

The EU1 lineage is a different mating type than the NA1 lineage already established in Oregon. Scientists should study P. ramorum populations in Vietnam and Japan, where both mating types are present, to determine whether they are reproducing sexually. There is also the risk that the EU1 lineage might be more aggressive on conifers – as it has been in the United Kingdom (Grünwald et al. 2019).

The EU1 infestation was introduced to the forest from a nursery. The nursery had carried out the APHIS-mandated Confirmed Nursery Protocol, then closed.  I ask, what does this apparent transmission from nursery to forest say about the risk of transmission? Does it raise questions about the efficacy of the confirmed nursery protocol to clean up the area? Remember that a pond at the botanical garden in Kitsap, Washington has repeatedly tested positive, despite several applications of the clean-up protocols.

(For a discussion of the implications of mixing the various strains of P. ramorum, visit here)

These disasters remind us how sad it is that California and federal officials did not adopt aggressive management efforts aimed at slowing the pathogen’s spread at an early stage of  the epidemic. Experts on modeling the epidemiology of plant disease concluded three years ago that the sudden oak death epidemic in California could have been slowed considerably if aggressive and well-funded management actions had started in 2002 (Cunniffe, Cobb, Meentemeyer, Rizzo, and Gilligan 2016).

The Oregon Department of Forestry commissioned a study of the economic impact of the P. ramorum infestation that found few economic impacts to date, but potentially significant impacts in the future. It also noted potential harms to tribal cultural values and the “existence value” of tanoak-dominated forests and associated obligate species.

Situation Abroad

The situation in Europe is even worse than in North America. Two strains of P. ramorum are widespread in European nurseries and in tree plantations and wild heathlands of western the United Kingdom and Ireland. and here and here.  Jung et al. 2015 found 56 Phytophthora taxa in 66% of 2,525 forest and landscape planting sites across Europe that were probably introduced to those sites via nursery plantings.

larch plantation in UK killed by P. ramorum
photo from UK Forest Research

In Australia, Phytophthora dieback has infected more than one million hectares in Western Australia. More than 40% of the native plant species of the region are vulnerable to the causal agent, P. cinnamomi

 and here.  

Barber et al. 2013 reported 9 species of Phytophthora associated with a wide variety of host species in urban streetscapes, parks, gardens, and remnant native vegetation in urban settings in Western Australia. Phytophthora species were recovered from 30% of sampled sites.

In New Zealand, the endemic – and huge, long-lived – kauri tree (Agathis australis) is also suffering severe impacts from Phytophtoras and other pathogens (Bradshaw et al. 2020)

See the IUFRO Working Party 7.02.09 ‘Phytophthora Diseases of Forest Trees’ global overview (Jung et al. 2018), which covers 13 outbreaks of Phytophthora-caused disease in forests and natural ecosystems of Europe, Australia and the Americas.

The situation in the Eastern United States is Unclear

After 15 years of the nursery trade carrying P. ramorum to nurseries – and possibly yards and other plantings – in states east of the 100th Meridian, what is the risk that these forests will become infested? No one knows. We do known that the pathogen has been detected from 11 streams in six eastern states – four in Alabama; one in Florida; two in Georgia; one in Mississippi; one in North Carolina; and two in Texas. P. ramorum has been found multiple times in eight of these streams – two steams in Alabama, one each in Mississippi and North Carolina (see COMTF April 2019 newsletter available here). While established vegetative infections have not been detected, the question remains: how is the pathogen persisting? Scientists agree that P. ramorum cannot persist in the water; it must be established on some plant parts (roots?) or in the soil. Still, Grünwald et al. (2019) report that there is little evidence of plant infections resulting from stream splash in Oregon.

Unfortunately, fewer states are participating in the stream surveys – which are operated by the USDA Forest Service. In 2010, 14 states participated; in 2018, only seven (Alabama, Georgia, Mississippi, North Carolina, Pennsylvania, South Carolina, and Texas). Florida and Tennessee recently dropped out. The number of streams surveyed annually also has dropped – from 95 at the highest to only 47 in 2018 (see COMTF April 2019 newsletter available here). This reduced scrutiny makes it less likely that any infestation on plants will be detected. Risk maps (reproduced in Chapter 5 of Fading Forests III here) developed over more than a decade indicate that forests in the southern Appalachians and Ozarks are vulnerable to SOD.

Risks to other plants

The risk from Phytophthoras is not just P. ramorum and trees! Swiecki et al. 2018 report a large and increasingly diverse suite of introduced Phytophthora species pose an ever greater threat to both urban and non-urban plant communities in California. These threats are linked to planting of nursery stock. See also the information posted here.

Jung et al. 2018 cite numerous other authors’ findings of multiple Phytophthoras in Oregon and. California nurseries as well as in nurseries in various eastern states.

Nor is Phytophthoras the only pathogenic genus to pose a serious risk to America’s trees. I remind you of the fungus Fusarium euwallacea associated with the Kuroshio and polyphagous shot hole borers, which is known to kill at least 18 species of native plants in California and additional species in South Africa.   The laurel wilt fungus kills many trees and shrubs in the Lauraceae family. ‘Ohi‘a or myrtle rust kills several shrubs native to Hawai`i and threatens a wide range of plants in the Myrtaceae family in Australia and New Zealand; rapid ‘ohi‘a death fungi (Ceratocystis huliohia and Ceratocystis lukuohia)  [All described here] are killing the most widespread tree on the Hawaiian Islands.

Solutions – complete & implement modernized international and domestic phytosanitary regulations

Clearly, standard phytosanitary practice of regulating pests known to pose a threat does not work when many – if not most – of the damaging pests are unknown to science until introduced to a naïve ecosystem where they start causing noticeable levels of damage. We need a more proactive approach – as has long been advocated by forest pathologists, including Clive Brasier 2008 and later, Santini et al. 2013, Jung et al. 2016, Eschen et al. 2017.

National and international phytosanitary agencies have taken some steps toward adopting policies and programs that all hope will be more effective in preventing the continued spread of these highly damaging tree-killing pests. First, APHIS has had authority since 2011 – through the Not Authorized for Importation Pending Pest Risk Assessment (NAPPRA) program — to prohibit temporarily imports of plants suspected of transporting known damaging pathogens until the agency has conducted a pest risk analysis. However, utilization has lagged: only three sets of species have been proposed for listing in NAPPRA in the eight and a half years since the program was instituted in 2011. The third list of proposed species is currently open for public comment.

Another weakness is that the program still focuses on organisms known to pose a risk.

Second, in 2018 APHIS completed a decades-long effort to revise its plant import regulations (the “Q-37” regulations). APHIS now has authority to require foreign suppliers of living plants to carry out “hazard analysis and critical control point” programs and adopt integrated pest management strategies to ensure that the plants are pest-free during production and transport.

However, implementation of this new authority depends on APHIS negotiating agreements with individual countries that would govern specific types of plants exported to the U.S. APHIS has not yet announced completion of any programs under this authority. Nor is it clear which taxa or countries APHIS will prioritize.

APHIS’ action was anticipated by the international plant health community. In 2012, member states in the International Plant Protection Convention adopted International Standard for Phytosanitary Measure 36 (ISPM#36)  The standard sets up a two-level system of integrated measures, which are to be applied depending on the pest risk identified through pest risk analysis or a similar process. The “general” integrated measures are widely applicable to all imported plants for planting. The second level includes additional elements designed to address higher pest-risk situations that have been identified through pest risk analysis or other similar processes. 

However, the preponderance of international efforts to protect plant health continues to rely on visual inspections that look for species on a list of those known to be harmful. Yet we know that most damaging Phytophthoras were unknown before their introduction to naïve ecosystems.

Furthermore, use of fungicides and fungistatic chemicals – that mask infections but do not kill that pathogen – is still allowed before shipment.

(For more complete analyses of the Q-37 revision and ISPM#36, see chapters five and four, respectively, of Fading Forests III.)

The nursery industry is working with state regulators and APHIS to develop a voluntary program utilizing  integrated measures – the Systems Approach to Nursery Certification (SANC) program. https://sanc.nationalplantboard.org/

SOURCES

Bradshaw et al. 2020. Phytophthora agathidicida: research progress, cultural perspectives and knowledge gaps in the control and management of kauri dieback in New Zealand. Plant Pathology (2020) 69, 3–16 Doi: 10.1111/ppa.13104

Brasier CM. 2008. The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathology 57: 792–808.

Brasier, C.M, S. Franceschini, A.M. Vettraino, E.M. Hansen, S. Green, C. Robin, J.F. Webber, and A.Vannini. 2012. Four phenotypically and phylogenetically distinct lineages in Phytophthora lateralis

Fungal Biology. Volume 116, Issue 12, December 2012, Pages 1232–1249

Campbell, F.T. Calculation by F.T. Campbell from tables in U.S. Department of Agriculture, Animal and Plant Health Inspection Service – National Plant Board.  2011.  Phytophthora ramorum Regulatory Working Group Reports.  January 2011.

Cunniffe, N.J., R.C. Cobb, R.K. Meentemeyer, D.M. Rizzo, and C.A. Gilligan. Modeling when, where, and how to manage a forest epidemic, motivated by SOD in Calif. PNAS, May 2016 DOI: 10.1073/pnas.1602153113

Grünwald, N.J., J.M. LeBoldus, and R.C. Hamelin. 2019. Ecology and Evolution of the Sudden Oak Death Pathogen Phytophthora ramorum. Annual Review of Phytopathology date? #?

Jung T, Orlikowski  L, Henricot B, et al. 2016. Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora diseases. Forest Pathology 46: 134–163.

Jung, T., A. Pérez-Sierra, A. Durán, M. Horta Jung, Y. Balci, B. Scanu. 2018. Canker and decline diseases caused by soil- and airborne Phytophthora species in forests and woodlands. Persoonia 40, 2018: 182–220   Open Access!

Jung, T. et al. 2015. Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora disease. Forest Pathology. November 2015; available from Resource Gate

Jung, T., B. Scanu, C.M. Brasier, J. Webber, I. Milenkovic, T. Corcobado, M. Tomšovský, M. Pánek, J. Bakonyi, C. Maia, A. Baccová, M. Raco, H. Rees, A. Pérez-Sierra & M. Horta Jung. 2020. A Survey in Natural Forest Ecosystems of Vietnam Reveals High Diversity of both New and Described Phytophthora Taxa including P. ramorum. Forests, 2020, 11, 93 https://gcc02.safelinks.protection.outlook.com/?url=https%3A%2F%2Fwww.mdpi.com%2F1999-4907%2F11%2F1%2F93%2Fpdf&data=02%7C01%7C%7Cfcd843919a3348a4a56108d7974039ab%7Ced5b36e701ee4ebc867ee03cfa0d4697%7C0%7C1%7C637144174418121741&sdata=WayrZsxp3P9Kj0h1aDPZnzu4yjDGA2ZEuH9NZITFQF4%3D&reserved=

Knaus, B.J., V.J. Fieland, N.J. Grunwald. 2015. Diversity of Foliar Phytophthora  Species on Rhododendron in Oregon Nurseries. Plant Disease Vol 99, No. 10 326 – 1332

Pfister, S. USDA APHIS. Presentation to the National Plant Board, August 2013

Porter, R.D. and N.C. Robertson. 2011. Tracking Implementation of the Special Need Request Process Under the Plant Protection Act. Environmental Law Reporter. 41.

Santini A, Ghelardini L, De Pace C, et al. 2013. Biogeographic patterns and determinants of invasion by alien forest pathogens in Europe. New Phytologist 197: 238–250.

Swiecki, T.J., E.A. Bernhardt, and S.J. Frankel. 2018. Phytophthora root disease and the need for clean nursery stock in urban forests: Part 1 Phytophthora invasions in the urban forest & beyond. Western Arborist Fall 2018

Tsao PH. 1990. Why many Phytophthora root rots and crown rots of tree and horticultural crops remain undetected

Sudden Oak Death update

P. ramorum-infected rhododendron plants
Indiana Department of Natural Resources

As you may remember, in June and July I blogged about a troubling outbreak of sudden oak death pathogen Phytophtora ramorum in the nursery trade. The discovery was made by Indiana authorities, who carefully inspected plants being sold in the state. They discovered that rhododendron plants imported from an Oklahoma wholesaler included infected plants.

By the end of May, Indiana state inspectors had destroyed more than 1,500 rhododendrons and prohibited sale of another 1,500 plants  pending determination of their health. [source: Indianapolis Star 29 May, 2019]  Over the next months, APHIS determined that more than 50 rhododendron plants found in Indiana nurseries had been infected [California Oak Mortality Task Force Newsletter August 2019 ].

In the spring and summer, APHIS and state authorities alerted 28 states that they might have received plants from the suspect sources – the suppliers of the Oklahoma wholesaler — one nursery in Washington State and two nurseries from Canada. In the end, APHIS determined that plants exposed to the pathogen had been sent to 18 states – Alabama, Arkansas, Iowa, Illinois, Indiana, Kansas, Kentucky, Michigan, Missouri, Nebraska, North Carolina, Ohio, Oklahoma, Pennsylvania, Tennessee, Texas, Virginia, and West Virginia. As of late July, P. ramorum-positive nursery stock had been detected in nurseries in seven of these (Iowa, Illinois. Indiana, Kansas, Missouri, Nebraska, Oklahoma) plus  Washington [California Oak Mortality Task Force Newsletter August 2019].

As I pointed out in the earlier blog, this is just the latest of several occasions since 2004 in which infected plants have been widely distributed by the nursery trade, despite federal and state regulations. Also, at the time of this outbreak, APHIS had just formalized several steps relaxing the regulations that had been implemented through Federal Orders adopted in recent years. (See the earlier blog for details.)

APHIS actions

I wonder at APHIS’ delay in explaining to stakeholders the situation– and what it is doing about it!  APHIS provided minimal information to me – by email rather than a public announcement; this email came a month after Indiana announced detection of the pathogen to the public (as reported in my blog).  APHIS issued an official notice even later, in mid-July [California Oak Mortality Task Force (COMTF) Newsletter August 2019]. Neither notice was timely, given the serious risks to both nursery and naturally growing plants from the pathogen.

It is now November and principal questions have not yet been answered. How did the inspection systems in Washington and British Columbia fail to detect the outbreaks before the plants were shipped? This lapse is especially worrisome because APHIS requires testing of soil and standing water, not just visual inspection of plants. Furthermore, rhododendrons are well known to be vulnerable to the pathogen and therefore are a specified focus of detection efforts!

The October COMTF newsletter includes a report by the Washington State Department of Agriculture that a nursery found positive in May will carry out a Critical Control Points (CCP) assessment. An “extensive fall certification survey” will also be conducted. Presumably, these efforts are aimed at determining how the outbreak occurred.

The Canadian Food Inspection Service (CFIA) described – briefly – its nationwide survey program. CFIA reported that one nursery was determined to be P. ramorum-positive in 2018, three in 2019. CFIA says that trace-forwards and trace-backs demonstrate that no Canadian nursery shipped infected plants to the U.S. in 2018 or 2019. So, apparently, none of the infected plants came from the Canadian nurseries.

I hope that Washington State and APHIS will soon determine the probable causes of the outbreak. APHIS should then promptly inform all stakeholders and engage them in developing improved programs and policies to minimize the likelihood that similar problems will occur again.

Phytosanitary officials from the states are apparently also seeking additional information from APHIS about what went wrong and how the agency plans to fix the problems. See the resolution adopted by the National Plant Board here

California Action

A much more positive development is that the California Department of Food and Agriculture (CDFA) has introduced a Voluntary P. ramorum Pre-Quarantine Program. This is a voluntary inspection program specifically for nurseries in California counties that are not currently regulated for the pathogen – but that might be put under regulation in the future. Inspections and sampling will be administered by county regulatory officials and samples will be processed by the CDFA Plant Pest Diagnostics Center. If P. ramorum is detected at a participating nursery, the PQP nursery may become a federally regulated establishment.

Broader Implications

As I pointed out in Fading Forests III, APHIS and the states have struggled to prevent spread of tree-killing pests once they have established in the country. Even regulated pests – such as Phytophthora ramorum and the emerald ash borer — have escaped the regulations. APHIS and/or the states have chosen not to engage on other pests, such as redbay ambrosia beetle and laurel wilt disease and the polyphagous and Kuroshio shot hole borers and associated Fusarium fungus. In other cases, some states have acted – and asked APHIS to not get involved – e.g., thousand cankers disease of walnut. This situation heightens the risk to our urban, rural, and wildland forests. Americans need a hard-nosed discussion of how we can improve coordinated efforts to prevent pests’ spread.

Posted by Faith Campbell

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