PHYTOPHTHORA OCCULTANS MAN IN’T VELD AND ROSENDAHL (2015)


California Pest Rating Proposal for

Phytophthora occultans Man In’t Veld and Rosendahl (2015)
Pest Rating: B

Comment Period: CLOSED


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  1. From: Elizabeth Bernhardt, Ph. D., Tedmund Swiecki, Ph.D. December 10, 2020
    Re: Review of: California Pest Rating Proposal for Phytophthora occultans Man in’t Veld and Rosendahl (2015), dated 11.03.20
    We offer the following comments for your consideration as you finalize the pest rating proposal.
    Initiating Event: We are concerned that that CDFA’s current system for dealing with first detections of potentially invasive and damaging pests is not adequate for taking timely actions to protect California agriculture and native vegetation. In the case of P. occultans, the first detection was made in June 2018 by CDFA’s lab, but apparently no action was taken for two years simply because the original sample was not “official”. Either more timely efforts need to be taken to obtain “official” samples after detections or unofficial but clearly credible detections need to be taken as prima facie evidence that the agent has been detected in the state. Note the type culture of P. occultans was isolated from cultivated American boxwood (Buxus sempervirens) and the first California detection was on cultivated B. microphylla.
    History & Status: Background: The following statement needs to be corrected for accuracy. “Since the discovery of Phytophthora ramorum, causal organism for the sudden oak death and Ramorum blight, there has been an increase of surveys in California and throughout the world for Phytophthora spp., which has resulted in the description of several new species.” Since the description of P. ramorum in 2001, dozens of new Phytophthora species have been described. According to: Hyun, I. H., & Choi, W. (2014). Phytophthora species, new threats to the plant health in Korea. The plant pathology journal, 30(4), 331–342. https://doi.org/10.5423/PPJ.RW.07.2014.0068, more than 50 species were described between 2000 and 2014, and many more have been identified since 2014. Ever-increasing numbers of previously unknown Phytophthora species have been circulating globally, facilitated primarily by the nursery plant trade. Plant health specialists globally have noted the threat that these pathogens pose to agriculture, forestry, horticulture, and natural vegetation.
    Hosts: Quercus douglasii and Umbellularia californica should be added to the host list. See notes under California distribution below.
    Symptoms: The description of disease progression is not accurate. According to the literature, the disease begins as a root rot and may eventually spread up to the root crown, opposite of what is described in the PRP. Gitto et al. 2018: “Affected plants exhibited decline and dieback in the canopy and had typical root rot symptoms.” The last sentence in this paragraph related to temperature, in which Agrios is cited, should be replaced by something species specific. In the species description paper, Man In’t Veld et al (2015) showed that P. occultans grew optimally on media from about 22 to 28 C, with a minimum growth temperature between 10 and 17 C and a maximum of 30 C, showing that it has wide adaptability to a range of temperatures. Reeser et al conducted pathogenicity tests at 20-22 C.
    California distribution: Sims et al also detected P. occultans in restoration nurseries in northern California between Jan 2015 and Sept 2016 . See: Sims, L.; Tjosvold, S.; Chambers, D.; Garbelotto, M. Control of Phytophthora species in plant stock for habitat restoration through best management practices. Plant Pathology 2019, 68, 196–204. In addition, Tyler Bourret and Heather Mehl at Rizzo Lab UC Davis Dept of Plant Pathology detected from roots of transplanted Quercus douglasii and Umbellularia californica in a restoration planting in Santa Clara county that they sampled in 2015. See Bourret, T.B. Efforts to detect exotic Phytophthora species reveal unexpected diversity. Chapter 2. Restoration outplantings of nursery‐origin Californian flora are heavily infested with Phytophthora. Ph.D. Thesis. University of California, Davis, CA. ProQuest Dissertations Publishing. 2018, 10746957. Based on the association of this pathogen with nursery stock and the lack of any concerted effort to detect it, it is likely that the CA distribution is considerably wider than these few detections indicate.

    Comment: Consequences of introduction 2) Known pest host range. In the limited detections that have been reported in the literature and noted above, P. occultans has been found on a variety of unrelated plant species in multiple families. Although there are no metrics in the PRP describing the differences in the host range categories, it would be safer to assume that the host range is wide. This would increase the category score to 3.
    Response: Usually a rating of 3 would include more diverse hosts. Some pathogens have host ranges including hundreds of species, and generally those are the ones to receive a 3.

    Comment 3) Pest Reproductive Potential. Assignment of the score 2 seems arbitrary based on what is known about Phytophthora reproduction and dispersal, and the fact that this particular species has apparently spread to many locations globally in a relatively short time. A 3 rating is more appropriate.
    Response: Pathogens that receive a 3 are usually spread with a vector and/or have a seed pathway.

    Comment: 4) Economic Impact Should add criterion B to the list. The pest will lower crop value by both causing disease and death of infected plants and by increasing nursery costs that will be needed to keep it out of nurseries. This would not change the economic impact score of 3.
    Response: Category B has been added.

    Comment: 5) Environmental impact: As noted above, P. occultans was also found on nursery-grown outplanted container plants of Umbellularia californica and Quercus douglasii in a restoration planting in Santa Clara county (Bourret 2018) and in a restoration nursery in northern California (Sims et al. 2019). Since this species has been recovered from wildland environments into which it has been introduced on nursery stock, it can clearly survive under these conditions. Hence, potential environmental impacts include B, C, and D as noted below. This would increase the environmental impact score to 3.
    B. The pest could directly affect threatened or endangered species. Phytophthora occultans appears to have a wide host range of woody plants. Reeser (2015) indicates several species of Ceanothus are susceptible, so it is entirely likely that endangered. Ceanothus species are susceptible to this species and will be at risk if P. occultans becomes more widespread. Impacts of several Phytophthora species to the endangered Ceanothus ferrisiae have already been documented in Santa Clara County (Swiecki, T. J.; Bernhardt, E. A. 2018 Evaluating threats posed by exotic Phytophthora species to endangered Coyote ceanothus and selected natural communities in the Santa Clara NCCP area. Final report. Prepared for Santa Clara Valley Habitat Agency. 135p.). Furthermore, Arctostaphylos uva-ursi is also susceptible (Reeser 2015), indicating that there is susceptibility within the genus Arctostaphylos. Native populations of several listed, threatened, or endangered manzanitas in northern California, including A. myrtifolia, A. pallida, A. densiflora, and A. hookeri ssp. ravenii are already being significantly impacted by other soil-borne Phytophthora species. Spread of P. occultans into habitats of rare manzanitas is likely to adversely affect their survival and habitat.
    C. The pest could impact threatened or endangered species by disrupting critical habitats. Given the wide host range of native plants (Reeser 2015) attacked by this host, it is reasonable to expect further spread would disrupt critical habitats.
    D. The pest could trigger additional official or private treatment programs. Agencies that manage restoration plantings have already instituted treatment programs for restoration plantings in which Phytophthora-infested plants have been unwittingly outplanted. This pathogen is likely to trigger further actions of this type if it becomes more widely spread. Consequences of Introduction to California for Phytophthora occultans: this pathogen has potential to have high impact. If the above score changes are made, the total score would be 15.
    Response: Thank you for the additional references, I am including more categories and increasing the score.

    Comment: 6) Post Entry Distribution and Survey Information: Unfortunately, this reliance on only official records leads to underestimation of risks to California vegetation. Sims et al. 2019 and Bourret 2018 show that this pest is moving in the nursery trade in California, but the actual extent of its distribution is unknown. In this case, the “low” rating is appropriate.
    Response: Yes it relies on official records and survey information, so it received a rating of “low”

    7) The final score: The final score underestimates the risks associated with this pathogen. The overall final score should be 14. Conclusion and Rating Justification: The proposed rating for Phytophthora occultans should be B.

    Comments from Tyler Bourret: December 13. 2020
    I see that CDFA is preparing another pest rating on a Phytophthora species, P. occultans. The CalPhytos working group is working on a comment, but I thought I’d just contact you with any technical detail I can provide about this species. This is a scary, anthropogenic hybrid that is clearly recently moving throughout the world through ornamental nursery industry and has widespread woody natives within its host range. I think a C rating is too low in my opinion.
    I (Rizzo lab in collaboration with Phytosphere) was actually the first to detect P. occultans in CA during our big 2015-16 SCVWD survey, but we had uncovered a species with more regulatory potential (P. quercina) and so some of our other finds were swept under the carpet. I also have failed to find the time to publish that survey outside of my dissertation, which is one of my major professional disappointments.
    We found another species closely related to P. citrophthora during our first Angeles National Forest survey in 2018 (CDFA has also seen this taxon too, I gave it the provisional name P. taxon eriodictyon) and I’ve been working on a manuscript to figure out how it was related to P. citrophthora. Well, in that manuscript I decided that P. taxon eriodictyon is another intraspecific lineage of P. citrophthora, but I also discovered that P. occultans is a hybrid between P. citrophthora and P. himalsilva. It’s embarrassing for the Dutch authors of P. occultans that they themselves failed to see that it was a hybrid (the big reason they didn’t notice what is fairly obvious is because of miscommunication within the Phytophthora community over what actual locus should be called “cox1/COI”). The same first author had recently published a paper describing a different Phytophthora hybrid.
    Anywho, here is a worldwide distribution of P. xoccultans based on GenBank accessions. Unfortunately, the ITS sequence of P. xoccultans is a P. himalsilva sequence – to get a species determination of P. xoccultans, it must have a P. himalsilva nuclear genome match and a P. citrophthora mitochondrial genome match. That means some of the ITS accessions could be either P. himalsilva or P. xoccultans – we can’t say for sure without a mitochondrial sequence. Also, there’s one strain in there that I haven’t uploaded the ITS of yet, so I’m the only one who knows about it until I upload it. Besides the CDFA finds, every other Californian P. occultans isolate is either from a restoration nursery or a restoration outplanting.
    Here’s my summary of the worldwide distribution of P. xoccultans, as of 2/2020. I can provide the specific sequence accessions if you’re interested.
    No of isolates: 21
    Countries / States: Belgium, CA, Germany, MA, Netherlands, OR, Poland, Taiwan, Turkey, WA
    Host / associated hosts / substrates: Acer, Achillea, Alnus, Berberis, Buxus, Ceanothus, Cornus, Quercus, Rhododendron, Umbellularia, water
    California isolations:
    Species Strain / Isolate Host / Substrate ITS mt Haplotype
    xoccultans SCVWD387 soil collected beneath Umbellularia californica need to upload (citrophthora)
    xoccultans SCVWD298 soil collected beneath Quercus douglasiana MG707804.1 (citrophthora)
    himalsilva or xoccultans WS-I89 / C2_85B_ACCI5_1 Acer circinatum (roots) MH171638.1 not uploaded
    -Tyler
    Response: Thank you for the information.

    Comments from Faith Campbell: December 14. 2020
    Subject: Comments on California Pest Rating Proposal for Phytophthora occultans
    The Center for Invasive Species Prevention (CISP) is pleased that the California Department of Food and Agriculture (CDFA) is assessing the pest risk ratings of several Phytophthora species recently determined to be present in California. We appreciate the opportunity at this time to comment on the proposed rating for Phytophthora occultans.
    We note that the CDFA proposes a “C” rating for Phytophthora occultans.
    We are troubled by this proposed rating, for the reasons stated below. We consider a “B” rating to be more appropriate.
    Background/Distribution

    Comment: 1) The data presented in the CDFA proposal are too limited to support a determination of the species’ distribution in California. While the proposal refers to only two detections, two years apart, the proposed ranking of “C” seems to imply that CDFA assumed the pathogen to be widespread. The available record does not indicate that CDFA carried out any surveys of other plants at the contractor’s nursery or at other nurseries or consultations with a larger group of stakeholders in an effort to clarify the pathogen’s current distribution
    Response: It received a score of ‘Low’ – pest has a localized distribution; or is established in one suitable climate/host area (region). I agree we don’t know if it is generally distributed in California.

    Comment: 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 in the case of other pathogens in the Phytophthora genus). If the host range expands, as we expect it will, the impact to restoration activities, rare plants, wildlands and nurseries is more likely to be significant, not medium to low. In particular, 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. We think it is highly unwise to disregard in risk assessments the probability that listed species will prove to be hosts.
    Response: In the Uncertainty section, I have included that the host range is likely to expand

    In conclusion, the Center for Invasive Species Prevention asks that the California Department of Food and Agriculture amend its proposal and assign a risk rating of “B” to Phytophthora occultans. Sincerely, Faith Thompson Campbell, Ph.D.

    Comment from Janice Alexander: December 14, 2020
    From: Phytophthoras in Native Habitats Work Group, http://www.calphytos.org,
    Subject: Comments on California Pest Rating Proposal for Phytophthora occultans
    The Phytophthoras in Native Habitats Work Group is pleased that the CDFA is assessing the pest risk ratings of several Phytophthora species; we appreciate the opportunity to comment as proposed ratings become available. Here we comment on the posted California Pest Rating Proposal for Phytophthora occultans which is proposed for a “C” rating. We see the “C” rating as problematic for this organism. We suggest it be assigned a “B” rating. A “C”-rating is for “pests of the agricultural industry or environment which score medium to low and are of common occurrence and generally distributed in California. Authorized mitigating regulatory actions: Plants and plant products found infested or infected with or exposed to a “C”-rated pest are not subject to any State enforced regulatory actions listed under subsection 3162(e)” (CHAPTER 5B-3 PLANT QUARANTINE).
    A “C” rating is inappropriate for P. occultans because:

    Comment: 1) Its distribution is not fully understood, there are few reports in California, and it is not known to be generally distributed in the state.
    Response: It received a score of ‘Low’ – pest has a localized distribution; or is established in one suitable climate/host area (region). I agree we don’t know if it is generally distributed in California.

    Comment: 2) Its impact to restoration activities, rare plants, wildland and nurseries is most likely not medium to low.
    Response: I have included more categories and increasing the score to high in this category based on previous, similar comments.

    Comment: According to the “C” rating definition, showing that either of these statements is true, would move the rating to “B”. A “B” rating would be beneficial to plant health in California because it would allow response action at the discretion of the County Agricultural Commissioner.
    Response: Both a B and a C rating are at the discretionary action of a CAC, only an A or Q rating trigger a State-directed quarantine response.

    Comment: In the risk rating proposal, the distribution and host list provided for P. occultans is limited but it has been found on a variety of unrelated plant species in multiple families. It logically follows that its current distribution is not common but there is the potential for damage to a broad range of hosts. We are particularly concerned that P. occultans could damage threatened or endangered species. Reeser and others (2015) indicate several species of Ceanothus are susceptible, so it is likely that endangered Ceanothus species are susceptible and would be further at risk if P. occultans becomes more widespread. Impacts of several Phytophthora species to the endangered Ceanothus ferrisiae have been documented in Santa Clara County. Substantial action, at significant expense, was undertaken to eradicate the pathogen from the soil and planting basins (Frankel and others 2020b). Arctostaphylos uva-ursi is also susceptible to P. occultans (Reeser and others 2015), indicating other species of Arctostaphylos (manzanita) may also be at risk. Native populations of several listed, threatened, or endangered manzanitas in northern California, including A. myrtifolia, A. pallida, A. densiflora, and A. hookeri ssp. ravenii are already being significantly impacted by other Phytophthora species (Frankel and others 2020a). Spread of P. occultans into habitats of rare manzanitas is likely to adversely affect these ecologically important plants. These show risk for greater than low or moderate impacts.
    Response: Thank you for the information, we can rely only on official samples for the score. A more widespread distribution would support a lower score in category 6. In the Uncertainty section, I have included that the host range is likely to expand and given citations.

    Thank you for considering these points. Please let us know if we may be of further assistance. For more information on Phytophthoras in California native plant nurseries and restoration sites, see http://www.calphytos.org, or contact Janice Alexander, UC Cooperative Extension, Marin Co. We look forward to continuing to work with you to sustain plant health for California.
    References
    Frankel, S. J.; Alexander, J.; Benner, D.;Hillman, J. and Shor, A. 2020a. Phytophthora pathogens threaten rare habitats and conservation plantings. Sibbaldia: the International Journal of Botanic Garden Horticulture, (18): 53-65.
    Frankel, S.J.; Conforti, C.; Hillman, J.; Ingolia, M.; Shor, A.; Benner, B. Alexander, J.A.; Bernhardt, E.; and Swiecki, T.J. 2020b. Phytophthora Pathogen Introductions in California Restoration areas: Protecting California Native Flora from Human-assisted Pathogen Spread. Forests. 11: 1291. doi: 10.3390/f11121291.
    Reeser, P.W.; Sutton, W.; Hansen, E.M.; Goheen, E.M., Fieland, V.J. and Grünwald, N.J. 2015. First report of Phytophthora occultans causing root and collar rot on Ceanothus, boxwood, rhododendron, and other hosts in horticultural nurseries in Oregon, USA. Plant Disease. 99(9).

    Comments from Jennifer Parke: December 18, 2020
    From: Jennifer Parke, Professor (Senior Research), Dept. of Crop and Soil Science and Dept. of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331 Email: Jennifer.Parke@oregonstate.edu
    Subject: Comments on California Pest Rating Proposal for Phytophthora occultans
    I am a plant pathologist at Oregon State University who has worked with Phytophthora species in agricultural and wildland settings for 36 years. I wish to comment on the proposed pest rating of “C” for Phytophthora occultans. I suggest that CDFA give it a “B” rating for the following reasons that pertain to the CDFA’s predicted consequences of introduction:

    Comment: Item 2. Known pest host range: Score 3. P. occultans is likely to have a wide host range, not a moderate host range. The known host range includes multiple species in the following genera: Acer, Arctostaphylos, Buxus, Ceanothus, Choisya, Gaultheria, Mahonia, Rhododendron, and Taxus. The pathogen appears to have emerged relatively recently in the nursery trade in Europe and the U.S. and so the host range is likely to be underestimated. The diversity of plant families already known to be affected by P. occultans suggests that many more woody plant species are likely susceptible to this pathogen.
    Response: Usually a rating of 3 would include more diverse hosts. Some pathogens have host ranges including hundreds of species, and generally those receive a 3. I have included comments on host range in the uncertainty section.

    Comment: Item 5. Environmental impact. Score 3. P. occultans has the potential to cause a high environmental impact, not a medium impact. P. occultans is known to cause disease on several native plant species (Arctostaphylos uva-ursi; Ceanothus sanguineus, C. velutinus, and C. integerrimus; Gaultheria shallon; and Mahonia nervosa). It is highly likely that additional members of these genera, including rare or endangered California native species of Arctostaphylos and Ceonothus, are susceptible to P. occultans. If P. occultans becomes established in California restoration nurseries, it could directly affect threatened or endangered species. The pathogen could also be spread with nursery stock to impact threatened or endangered species and disrupt critical habitats.
    Response: Thank you for your comments, I have received similar previous comments and added to the environmental impact section.

    Comment: Item 6. Post Entry Distribution and Survey Information. Score 0. There is no evidence that P. occultans is established in California. The pathogen was only isolated twice, despite intense surveys for Phytophthora species in nurseries, landscapes and wildlands during the last 19 years. Thus, the potential for limiting establishment through regulation is high.
    Response: I can only use Not Established (0) for “a Pest never detected in California or known only from incursions”. Since P. occultans was found in a landscape and in California nursery stock, and it is not under state eradication, I need to give it a score of Low (-1) for “Pest has a localized distribution in California or is established in one suitable climate/host area (region)”.

    Consideration of these suggestions would result in a final score of 14, justifying a “B” rating in Phytophthora occultans.
    Thank you for the opportunity to comment.

    Response: After considering the Pest Risk Proposal and the comments, the following rating is recommended: Rating: B

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