2 thoughts on “Phytophthora mediterranea C. Bregant, Mulas & Linald. (2021)”

1. Response to Comments from Elizabeth Bernhardt, Ph. D., Tedmund Swiecki, Ph.D., Phytosphere Research
   Re: Comments on California Pest Rating Proposal for Phytophthora mediterranea C. Bregant, Mulas & Linald. (2021)
   Comment: Initiating Event / Background: As we have noted in previous comments on CDFA PRP (Comments on PRP for Phytophthora occultans, dated 12/10/2020), 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.
   As noted under the PRP Background heading, Troullais et al. (2022) published data indicating that P. mediterranea was present in commercial pistachio and almond orchards that were sampled between 2015 and 2018. Beyond this, CDFA Analysis and Lab received Phytophthora mediterranea isolates (then unnamed) that we submitted for identification in fall of 2016 (PDR MV6P06578691, MV6P06578692). The CDFA lab sequenced multiple loci and concluded that these isolates were likely a new or hybrid species closely related to P. cinnamomi and P. parvispora. We had baited these isolates from the roots of recently killed Quercus agrifolia nursery stock that had been transplanted into a restoration site in the Angeles National Forest. Hence, CDFA had information on the presence of this novel species in California three years before Bregant et al. (2021) collected their first isolates in Italy from Myrtis communis and later applied the name P. mediterranea. The ability to prevent the spread of this pathogen into agriculture and native ecosystems in California has been severely compromised by the gap of more than 8 years between its initial CDFA identification and the current Pest Rating Proposal, which was initiated only after the August 2024 detection from nursery stock.
   For the sake of accuracy, these details should be added to the background (History and Status section). Furthermore, P. mediterranea was recovered from dead or dying Q. agrifolia nursery stock at the same Angeles NF restoration site in 2019 (sampling conducted by David Rizzo’s lab, UC Davis) and in 2021 (further sampling conducted by Phytosphere Research). Those sample results are presented in Swiecki and Bernhardt (2016, 2021) and Bourret et al (2021).
   Response: About activities and detections made between 2015 and 2021; Pest rating proposals support responses and other activities, but we do not necessarily need to wait for one to respond and take action. Our diagnostic pathologists assign the initial rating, based on the apparent distribution and the likely risks, and in this case, a rating of Z was appropriate. If they had felt it warranted a Q- rating, immediate quarantine action could have been taken. Specifically for the PDRs you cite, there is always the question of pathogenicity when isolates are collected by baiting, and we do not use this method in our lab. We are unable to take action on finds where the taxonomy of the pathogen is incomplete or unknown. Work such as phylogenetic research or host range determinations are beyond the scope of our lab

   Comment: History & Status: Hosts: Repeated recoveries of this pathogen over multiple years from symptomatic plants as noted in Swiecki and Bernhardt (2021) and Bourret et al (2021) appear to indicate that Quercus agrifolia is a host of P. mediterranea. Bourret et al. (2021) also notes that P. mediterranea (originally provisionally identified as P. cinnamomi) was also recovered from Salvia rosmarinus from a southern California commercial nursery.
   Response: I do not have access to documents such as reports prepared for the US Forest Service or Phytosphere Research. Similar to my comments above, these would not be official samples nor are they considered published literature. We do collaborate with phylogenetic experts such as yourselves and Dr. Bourret at the USDA, within our mutual limits on time and resources. I appreciate you sharing your experience and expertise with CDFA – here it expands our knowledge of this pathogen in California.
   Comment: Damage potential: The apparent pathogenicity of P. mediterranea to Quercus agrifolia indicates that this species has the potential to affect at least this widespread and ecologically important native oak. The limited information on the pathogenicity of this species is unlikely to reflect its actual host range. The fact that P. mediterranea is already associated with hosts in the Anacardiaceae, Fagaceae, Lamiaceae, Myrtaceae, Proteaceae, and Rosaceae suggests that it has a potentially wide host range. Furthermore, this species is closely related to P. cinnamomi, which has the widest documented host range of any Phytophthora species. P. mediterranea is likely to cause plant decline and mortality in highly susceptible hosts.
   Response: Although this section allows for some speculation, I do not have adequate citations for direct damage to Q. agrifolia, citations to predict damage to a broad number of species at the family level, or evidence that the pathogenicity of P. mediterranea compares to that of P. cinnamomi.
   Comment: Consequences of introduction 1) Climate/Host Interaction. Given that this species has been shown to persist in southern California and in the Central Valley and was also detected in the San Francisco Bay area, a high (3) rating is appropriate. The limited distribution data available to date do indicate that this species could function over much of California.
   Response: I have no official or formally published records from Southern California. Central Valley and Bay Area detections together give a score of medium (2).
   Comment: 2) Known pest host range. In the limited detections that have been reported in the literature and noted above, P. mediterranea 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, especially given the close relationship to P. cinnamomi. The score for this rating should be increased to high (3).
   Response: In this section, I can only report on the observed host range (published in literature with pathogenicity established) which limits me to these 3 plants. A score of medium (2) is appropriate.
   Comment: 3) Pest Reproductive Potential. Assignment of the score 2 seems inconsistent with what is known about Phytophthora reproduction and dispersal, and the fact that this particular species has apparently spread to distant locations globally in a relatively short time. The score for this rating should be increased to high (3).
   Response: This section considers broadly the ways that pathogens can reproduce. Generally, I give a score of 3 to those phytopthoras with the ability to reproduce on multiple parts of their hosts, sometimes above and below ground, and with all possible spore types. For example, P. ramorum receives a 3 in this category because it can infect roots, crowns, trunks, and leaves, it has waterborne and aerial spores, and it produces oospores in addition to sporangia, zoospores and chlamydospores. This species is limited to roots and root collars, and oospores are not known to occur/play a role in pathogenicity. A score of medium (2) is appropriate.
   Comment: 4) Economic Impact. Criteria B and D should be added to the list. The pest will lower crop value by both causing disease and death of infected plants in the field and by increasing nursery costs and requiring changes in cultural practices needed to keep it out of nurseries. This would change the economic impact score to 3.
   Response: I agree this pathogen could lower crop value if the cost of removing dead and dying trees is considered and I have added (B). There are multiple species of Phytophthora already widely present in all types of nurseries and in our deciduous fruit and nut tree orchards in California. I don’t think a specific diagnosis of this species would change cultural practices significantly. With the addition of one more criterion to this section, the score has been changed from medium (2) to high (3).
   Comment: 5) Environmental impact. This species has been shown to persist in wildland environments for more than 5 years after its introduction on infested nursery stock, clearly indicating that it has the potential to affect native habitats, including those that support threatened or endangered species. The closely related species P. cinnamomi has been shown to directly affect multiple endangered Arctostaphylos species and other threatened or endangered species in California (Swiecki et al 2011, Frankel et al 2020), which have triggered both official and private treatment programs to limit further spread. P. mediterranea has the potential to express similar levels of pathogenicity to multiple California native species, causing habitat reduction and degradation. Hence, potential environmental impacts include B, C, and D. This would change the environmental impact score to 3.
   Response: There is limited information on the persistence of P. mediterranea in natural systems. Although this section does allow for reasonable conjecture, having a close taxonomic relatedness to another Phytophthora species does not inevitably lead to a similar level of pathogenicity. At this moment, the known host range established by official samples and pathogenicity testing is small, and none of these hosts are native to California. A score of medium (2) is appropriate.
   Comment: Consequences of Introduction to California for Phytophthora mediterranea: This pathogen has potential to have high impact. If the above score changes are made, the total score would be 15.
   Response: The score has increased by 1 point to 11, which is in the medium range (9-12).
   Comment: 6) Post Entry Distribution and Survey Information: Because no targeted surveillance to detect this species has occurred, official detection records underestimate the risks it poses to California vegetation. Available data clearly show that this pathogen has been moving in the nursery trade in California and elsewhere, but the actual extent of its distribution is unknown. In this case, the “low” rating is appropriate.
   Response: Agreed, no change to this section
   Comment: 7) The final score. The final score underestimates the risks associated with this pathogen. The overall final score should be 14.
   Response: the final score is now 10.
   Comment: Uncertainty. This statement should be revised based on the southern California sampling of nursery stock. California data cited here suggest that P. mediterranea has been circulating in multiple California nurseries for at least 10 years. Like other Phytophthora species that circulate in California nursery stock, this increases the likelihood that P. mediterranea will be introduced into a variety of agricultural, landscape, and wildland situations over time. The lag period between Phytophthora introductions and obvious impacts to vegetation can be many years. The lack of regulation of Phytophthora species like P. mediterranea in nursery stock virtually ensures that these destructive invasive pathogens will become increasingly widespread, resulting in further degradation of native ecosystems, cultivated landscapes, and agricultural fields.
   Response: I share your feeling that P. mediterranea has likely been circulating in California nurseries for a long time. It was possibly misidentified as P. cinnamomi or only identified to the genus level, as the sp. nov. was not described until 2021. Its widespread presence in mature orchards in the Central Valley implies that even 10 years could be a significant underestimation of its tenure in California. Official and unofficial records from diverse locations and hosts in the state, and the impracticality of survey and eradication are all factors to consider. There is a high likelihood that it has had abundant time to be introduced into a variety of agricultural, landscape, and wildland situations. However, it has not been reported as such, or the reports are co-mingled with P. cinnamomi, which has always been a non-quarantine species. Once a pathogen is widespread in the nursery trades and perennial crops such as fruit trees over a wide area, imposing a B rating, which requires the pathogen to be eradicated from nursery blocks, it becomes very difficult; a significant burden with a low chance of achieving the desired outcome for stakeholders.
   Comment: Conclusion and Rating Justification: Based on the foregoing, the proposed rating for Phytophthora mediterranea should be B.
   Response: From the Primary State Plant Pathologist, the rating for Phytophthora mediterranea is C.

2. 07 January 2025

   To: Heather Martin
   From: Elizabeth A. Bernhardt, Ph. D., Tedmund J. Swiecki, Ph.D.
   Phytosphere Research, Vacaville, CA
   Phytosphere@phytosphere.com

   Re: Comments on California Pest Rating Proposal for Phytophthora mediterranea C. Bregant, Mulas & Linald. (2021), dated 12/05/24

   We offer the following comments for your consideration as you finalize the pest rating proposal.
   Initiating Event / Background:
   As we have noted in previous comments on CDFA PRP (Comments on PRP for Phytophthora occultans, dated 12/10/2020), 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.
   As noted under the PRP Background heading, Troullais et al. (2022) published data indicating that P. mediterranea was present in commercial pistachio and almond orchards that were sampled between 2015 and 2018. Beyond this, CDFA Analysis and Lab received Phytophthora mediterranea isolates (then unnamed) that we submitted for identification in fall of 2016 (PDR MV6P06578691, MV6P06578692). The CDFA lab sequenced multiple loci and concluded that these isolates were likely a new or hybrid species closely related to P. cinnamomi and P. parvispora. We had baited these isolates from the roots of recently killed Quercus agrifolia nursery stock that had been transplanted into a restoration site in the Angeles National Forest. Hence, CDFA had information on the presence of this novel species in California three years before Bregant et al. (2021) collected their first isolates in Italy from Myrtis communis and later applied the name P. mediterranea. The ability to prevent the spread of this pathogen into agriculture and native ecosystems in California has been severely compromised by the gap of more than 8 years between its initial CDFA identification and the current Pest Rating Proposal, which was initiated only after the August 2024 detection from nursery stock.
   For the sake of accuracy, these details should be added to the background (History and Status section). Furthermore, P. mediterranea was recovered from dead or dying Q. agrifolia nursery stock at the same Angeles NF restoration site in 2019 (sampling conducted by David Rizzo’s lab, UC Davis) and in 2021 (further sampling conducted by Phytosphere Research). Those sample results are presented in Swiecki and Bernhardt (2016, 2021) and Bourret et al (2021).
   History & Status:
   Hosts:
   Repeated recoveries of this pathogen over multiple years from symptomatic plants as noted in Swiecki and Bernhardt (2021) and Bourret et al (2021) appear to indicate that Quercus agrifolia is a host of P. mediterranea. Bourret et al. (2021) also notes that P. mediterranea (originally provisionally identified as P. cinnamomi) was also recovered from Salvia rosmarinus from a southern California commercial nursery.
   Damage potential:
   The apparent pathogenicity of P. mediterranea to Quercus agrifolia indicates that this species has the potential to affect at least this widespread and ecologically important native oak. The limited information on the pathogenicity of this species is unlikely to reflect its actual host range. The fact that P. mediterranea is already associated with hosts in the Anacardiaceae, Fagaceae, Lamiaceae, Myrtaceae, Proteaceae, and Rosaceae suggests that it has a potentially wide host range. Furthermore, this species is closely related to P. cinnamomi, which has the widest documented host range of any Phytophthora species. P. mediterranea is likely to cause plant decline and mortality in highly susceptible hosts.

   Consequences of introduction
   1) Climate/Host Interaction
   Given that this species has been shown to persist in southern California and in the Central Valley and was also detected in the San Francisco Bay area, a high (3) rating is appropriate. The limited distribution data available to date do indicate that this species could function over much of California.
   2) Known pest host range.
   In the limited detections that have been reported in the literature and noted above, P. mediterranea 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, especially given the close relationship to P. cinnamomi. The score for this rating should be increased to high (3).
   3) Pest Reproductive Potential.
   Assignment of the score 2 seems inconsistent with what is known about Phytophthora reproduction and dispersal, and the fact that this particular species has apparently spread to distant locations globally in a relatively short time. The score for this rating should be increased to high (3).
   4) Economic Impact
   Criteria B and D should be added to the list. The pest will lower crop value by both causing disease and death of infected plants in the field and by increasing nursery costs and requiring changes in cultural practices needed to keep it out of nurseries. This would change the economic impact score to 3.
   5) Environmental impact
   This species has been shown to persist in wildland environments for more than 5 years after its introduction on infested nursery stock, clearly indicating that it has the potential to affect native habitats, including those that support threatened or endangered species. The closely related species P. cinnamomi has been shown to directly affect multiple endangered Arctostaphylos species and other threatened or endangered species in California (Swiecki et al 2011, Frankel et al 2020), which have triggered both official and private treatment programs to limit further spread. P. mediterranea has the potential to express similar levels of pathogenicity to multiple California native species, causing habitat reduction and degradation. Hence, potential environmental impacts include B, C, and D. This would change the environmental impact score to 3.
   Consequences of Introduction to California for Phytophthora mediterranea:
   This pathogen has potential to have high impact. If the above score changes are made, the total score would be 15.
   6) Post Entry Distribution and Survey Information:
   Because no targeted surveillance to detect this species has occurred, official detection records underestimate the risks it poses to California vegetation. Available data clearly show that this pathogen has been moving in the nursery trade in California and elsewhere, but the actual extent of its distribution is unknown. In this case, the “low” rating is appropriate.
   7) The final score
   The final score underestimates the risks associated with this pathogen. The overall final score should be 14.
   Uncertainty
   This statement should be revised based on the southern California sampling of nursery stock. California data cited here suggest that P. mediterranea has been circulating in multiple California nurseries for at least 10 years. Like other Phytophthora species that circulate in California nursery stock, this increases the likelihood that P. mediterranea will be introduced into a variety of agricultural, landscape, and wildland situations over time. The lag period between Phytophthora introductions and obvious impacts to vegetation can be many years. The lack of regulation of Phytophthora species like P. mediterranea in nursery stock virtually ensures that these destructive invasive pathogens will become increasingly widespread, resulting in further degradation of native ecosystems, cultivated landscapes, and agricultural fields.
   Conclusion and Rating Justification:
   Based on the foregoing, the proposed rating for Phytophthora mediterranea should be B.

   References cited
   Bourret, T., Fajardo, S., Rizzo, D., Frankel, S., Swiecki, T., Bernhardt, E. 2021. Plant pathogen monitoring in Angeles National Forest restoration areas, Southern California Edison sites–May 2021 survey results and 2016 – 2021 summary findings. University of California, Davis and Phytosphere Research. Prepared for USDA-Forest Service.
   Frankel, S. J.; Conforti, C.; Hillman, J.; Ingolia, M.; Shor, A.; Benner, D.; Alexander, J. M.; Bernhardt, E.; Swiecki, T. J. 2020. Phytophthora introductions in restoration areas: Responding to protect California native flora from human-assisted pathogen spread. Forests 11:1291. https://doi.org/10.3390/f11121291.
   Swiecki, T.J., Bernhardt, E.A. 2016. Sampling for the presence of soil-borne Phytophthora species in selected southern California restoration sites and nurseries. Vacaville, CA: Phytosphere Research. Progress report prepared for USDA-Forest Service under Agreement No. 15-JV-11272131-076 Mod. 2.
   Swiecki, T.J., Bernhardt, E.A. 2021. Phytophthora monitoring plan for nursery stock and restoration sites to protect vegetation on the Angeles National Forest – Nursery stock prevention and monitoring. Final performance report. Vacaville, CA: Phytosphere Research. Progress report prepared for USDA-Forest Service under Agreement No. 18-JV-11272139-028
   Swiecki, T. J.; Bernhardt, E.; Garbelotto, M.; Fichtner, E. 2011. The exotic plant pathogen Phytophthora cinnamomi: A major threat to rare Arctostaphylos and much more. pp. 367–371. J. W. Willoughby, B. K. Orr, K.A. Schierenbeck, and N. J. Jensen [eds.], Proceedings of the CNPS Conservation Conference: Strategies and Solutions, 17–19 Jan 2009, California Native Plant Society, Sacramento, CA

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