Phytophthora cambivora | Pest Rating Proposals and Final Ratings

California Pest Rating for

Phytophthora cambivora (Petri) Buisman 1927

Pest Rating: B

PEST RATING PROFILE

Initiating Event:

None. The current risk and status of Phytophthora cambivora in California are reassessed and a permanent rating is proposed.

History & Status:

Background: Phytophthora cambiv ora is an oomycete pathogen that can cause crown and root rot disease, usually in conjunction with other Phytophthora spp., in its hosts. Phytophthora root and crown rot disease are among the most important soilborne diseases of stone fruits (Browne & Mircetich, 1995). The pathogen is known to cause ink disease in chestnut. It is widespread in temperate regions of all continents and occurs in soils of natural forests, agricultural fields, and orchards. It can persist and spread in different environments and is capable of surviving in the soil as a saprophyte and by producing resting spores.

In California, P. cambivora has been found in several fruit and nut, forest, and native host plants, including: apple, avocado, American plum, apricot, chamise, hoary manzanita, palm, birchleaf mountain mahogany, apple avocado, American plum, apricot, sweet cherry, cherry plum, sour cherry, European plum, sweet almond, holly leaf cherry, Mahaleb cherry, peach, nectarine, Japanese plum, European/common pear, oak, canyon oak, California live oak, Japanese maple, toyon, madrone, bristlecone fir (French, 1989, CDFA Pest Damage Records). Phytophthora diagnostic scientists have also found P. cambivora in other symptomatic (damaged) native plant species in natural stands in California. These unpublished records of P. cambivora-infected native plants include, Ione manzanita (Arctostaphylos myrtifolia), sticky white leaf manzanita (A. viscida), pallid manzanita (A. pallida), Raiche’s manzanita (A. stanfordiana ssp. raichei), coyote ceanothus (Ceanothus ferriseae), valley oak (Quercus lobata), and California coffeeberry (Frangula californica) (comments from S. Frankel, plant pathologist, USDA Forest Service, and ‘Phytophthoras in Native Habitats Work Group’. July, 2017). The pathogen has also been recovered from various habitats including flowing water, stream and ditch banks, edges of roadsides and highways, forests, residential gardens, parks, cemeteries, recreational areas, and nurseries.

Saavedra et al., (2007) reported decline and mortality of golden chinquapin trees (Chrysolepis chrysophylla) in parts of northern and north-western California, similar to the damage caused by P. cambivora on the same host in Oregon. The native range for this host species extends through the Coast Range Mountains from San Luis Obispo County, California, to Benton County, Oregon.

Recently, Jung et al., (2016) demonstrated by phylogenetic analysis that Phytophthora cambivora is a natural interspecific hybrid (a cross between two different Phytophthora species) in ITS Clade 7a, and, therefore, suggested that its name be changed to P. xcambivora. Hybrid Phytophthora are often more aggressive than their parental species and fare better in nurseries and out-planted settings. Furthermore, P. xcambivora (= P cambivora) is the most thermo-tolerant of all species in Clade 7a, with the ability to grow at temperatures greater that 35°C. This ability to grow at high temperatures enables the pathogen to grow in warm climates in California.

Hosts: Reported hosts of Phytophthora cambivora are present in 30 genera in 19 families: Abies bracteata (bristlecone fir), A. fraseri (fraser fir), A. procera (noble fir), Abies sp., Acer palmatum (Japanese maple), A. pennsylvanicum (striped maple), A. platanoides (Norway maple), A. rubrum (red maple), A. saccharum (sugar maple) , Acer sp., Adenostoma fasciculatum (chamise), Aesculus hippocastanum (horse chestnut), Alnus cordata (alder), A. rubra (red alder), Arbutus menziesii (madrone), Arctostaphylos canescens subsp. canescens (hoary manzanita), Areca sp. (palm), Castanea sp. (chestnut), C. crenata (Japanese chestnut), C. dentata (American chestnut), C. mollissima (Chinese chestnut), C. pumila (allegheny chinquapin), C. sativa (chestnut), Castanea x coudercii (Couderc chestnut), Casuarina equisetifolia (casuarina), Cercocarpus betuloides (island mountain mahogany), C. montanus var. glaber (birchleaf mountain mahogany), Chamaecyparis lawsoniana (Port Orford cedar), Chamaecyparis sp. (cypress/false cypress), Chrysanthemum cinerariifolium (pyrethrum), Chrysolepis chrysophylla (giant chinquapin), Cineraria sp., Dahlia campanulata (weeping tree dahlia), Erica sp., Eucalyptus sp. (eucalyptus), Fagus sp. (beech), F. sylvatica (common beech), Ficus carica (common fig), Heteromeles arbutifolia (toyon), Impatiens hawker (New Guinea impatiens), Juglans regia (English walnut), Juglans sp. (walnuts), Lithocarpus densiflorus (tanoak), Lobelia erinus (lobelia), Lupinus sp. (lupine), L. albus (white lupine), Malus sp. (ornamental species apple), M. domestica (apple), M. pumila var. domestica (apple), M. pumila var. dulcissima, M. sylvestris (European crab apple), Nothofagus sp. (southern beeches), Persea americana (avocado), Petunia parviflora (seaside petunia), Pieris sp., P. japonica (lily-of-the-valley shrub), Pisum sp., P. sativum (pea), Pistacia vera (pistachio), Poncirus trifoliata (hardy orange), Prunus sp., P. americana (American plum), P. amygdalus (almond), P. armeniaca (apricot), P. avium (sweet cherry), P. campanulata (Taiwan cherry), P. cerasifera (cherry plum), P. cerasus (sour cherry), P. domestica (European plum), P. dulcis (sweet almond), P. ilicifolia (hollyleaf cherry), P. mahaleb (Mahaleb cherry), P. persica (peach), P. persica var nectarina (nectarine), P. salicina (Japanese plum), Pyrus communis (European pear), P. serotina (black cherry), Quercus sp. (oak), Q. cerris (European Turkey oak) Q. agrifolia (California live oak), Q. alba (white oak), Q. chrysolepis (canyon oak), Q. macrocarpa (bur oak), Q. petraea (durmast oak), Q. ilex (holm oak), Q. robur (common oak), Q. rubra (northern red oak), Q. pubescens (downy oak), Rhododendron sp. (azalea), R. ponticum (common rhododendron), Rubus idaeus (American red raspberry), Senecio sp. (groundsel), S. cruentus, soil, Solanum tuberosum (potato), Tanacetum cinerariifolium (Pyrethrum), Taxus baccata (English yew), Ulmus sp. (elms), Vaccinium macrocarpon (cranberry), Vitis vinifera (grapevine) (CABI, 2017; Farr & Rossman, 2017; French, 1989).

Symptoms: Phytophthora cambivora, along with other Phytophthora species, cause root and crown rot disease of walnut, cherry, apple, peach, plum, and apricot (CABI, 2017). The expression of symptoms is dependent on the amount of root and crown tissue affected and speed of destruction. Usually, crown rots advance rapidly and trees fall and die soon after the first warm weather of spring, while their leaves wilt, dry, and remain attached to the tree (Adaskaveg et al., 2009). During early stages of infection, infected trees are difficult to differentiate from healthy, non-infected ones. However, as the infection progresses, the leaves become small, chlorotic, and droopy, and grow slowly on terminal shoots. A decline of infected trees sets in and sometimes trees without detectable symptoms die in early summer. Collar and root rot may occur in the same tree. Symptoms of P. cambivora often resemble those caused by other root rot or collar rot pathogens. Collar rot is exhibited as decayed bark at the base of the trunk and can start at several points simultaneously, progressing until the lower part of the trunk is completely girdled. Infected roots turn brown, brittle, and necrotic. Infected root systems resulting in necrosis of lateral roots and taproots can affect top growth. Vigorous trees with affected roots may not show appreciable crown symptoms (CABI, 2017). Chronic infections, mainly of roots, cause reduction in growth, early senescence, and leaf fall, and may remain unthrifty for several years before succumbing to the disease. Infected young trees are usually killed due to their small root systems and crown areas (Adaskaveg et al., 2015).

Disease development: Similar to most other Phytophthora spp., P. cambivora survives in the soil in the form of mycelium, sporangia, zoospores and oospores, and thrives in poorly-drained, water-saturated soils. It lives as a saprophyte in litter and in soil containing dead organic material and is favored by moist and moderate climates in a wide range of pH: 3.8-7. It is not resistant to drought. Optimum temperature range for growth is 22-24°C and maximum temperature (cessation of growth) is >32°C (CABI, 2017). Jung et al., (2016), reported the ability for P. xcambivora (= P. cambivora) to grow at temperatures greater that 35°C.

Sporangia and zoospores of P. cambivora in humid soils are the main source of infection. Sporangia are produced abundantly by young mycelia, which become sterile when they are more than 1 month old. P. cambivora produces sporangia from 9 to 30°C. Most sporangia are found on the ground surface in leaves, petals, or earthworm castings; within the upper 6 cm of soil, and near the crowns of trees (Cox, 2014). Sporangia can germinate directly or, more commonly in P. cambivora, indirectly by producing zoospores at 9-27°C. Zoospores allow a population to increase rapidly and disperse widely in films of free water. Zoospores are expelled from sporangia under suitable temperature and moisture conditions and swim by means of their flagella towards their host in response to root exudates. Once a zoospore comes in contact with a root, it germinates producing a germ tube, which penetrates the root directly under waterlogged soil conditions. More mycelium develops, and eventually, oospores (sexual spores) are produced, and serve as resting structures that can survive for several years. Phytophthora cambivora does not produce chlamydospores (thick-walled, asexual spores) (CABI, 2017).

Transmission: Like most Phytophthora species, P. cambivora is soil-borne and water-borne and may be spread to non-infected sites through infected plants, nursery and planting stock, and seedlings, soil, run-off and splash irrigation and rain water, and contaminated cultivation equipment, tools, and boots. The pathogen is not seed-borne but can be spread by infected seedlings (CABI, 2017). Irrigation water from canals, rivers, and ponds can be contaminated with Phytophthora spp. (Browne & Mircetich, 1995).

Damage Potential: Damage caused by Phytophthora cambivora alone may be difficult to assess as more than one species of Phytophthora may be associated with root and crown rot of host trees (Mircetich & Matherton, 1976). Loss of production of apple, cherry, noble fir Christmas trees have been reported from North America (CABI, 2017). Walnut, peach, plum and apricot are also susceptible to P. cambivora and other Phytophthora spp. Nurseries, nursery stock and ornamental productions may be at risk and need to be monitored.

California’s native vegetation is also at risk of root and crown rot caused by P. cambivora and other Phytophthora spp., many of which are endemic (limited) to the State, while some are rare, endangered, or threatened plants, e.g., pallid manzanita, Ione manzanita, sticky white leaf manzanita, valley oak, bristlecone fir, coffeeberry, etc. (CNPS, 2017; Calflora, 2017). Introduction of Phytophthora species are a threat to plant health in Bay Area restoration sites, where nursery stock is planted for flood control or to mitigate environmental impacts. Detections on madrone, toyon, oaks, and manzanitas in native stands indicate that P. cambivora is capable of becoming established in a variety of native plant habitats under a range of soil and environmental conditions and can have negative impacts on native vegetation (comments from S. Frankel, plant pathologist, USDA Forest Service, and Phytophthoras in Native Habitats Work Group. July, 2017).

Worldwide Distribution: Asia: India, Japan, Republic of Korea, Malaysia, Taiwan, Turkey; Africa: Madagascar, Mauritius, Nigeria, South Africa; North America: Canada, USA; Europe: Austria, Belgium, Croatia, Czech Republic, Denmark, France, Germany, Greece, Hungary, Ireland, Italy, Netherlands, Norway, Poland, Portugal, Romania, Russian Federation, Serbia, Slovakia, Slovenia, Spain, Sweden, Switzerland, United Kingdom, Yugoslavia (former); Oceania: Australia, New Zealand, Papua New Guinea (CABI, 2017).

In the USA it has been reported from Alabama, Arizona, Arkansas, California, Georgia, Maryland, Michigan, Minnesota, Missouri, Montana, New Jersey, New York, North Carolina, Ohio, Oklahoma, Oregon, Pennsylvania, South Carolina, Virginia, Washington, West Virginia (CABI, 2017).

Official Control: Presently, Phytophthora cambivora is on the “Harmful Organism Lists” for Algeria, Canada, Chile, China, Honduras, Nicaragua, and Peru, while, Phytophthora spp. is on the “Harmful Organism Lists” for Peru and South Africa (USDA PCIT, 2017).

California Distribution: Phytophthora cambivora is widely distributed within California. From 2013-April, 2017, the pathogen was officially detected in Alameda, Contra Costa, Marin, Monterey, Orange, Plumas, San Mateo, San Francisco, Santa Clara, Solano, and Sonoma Counties (CDFA Pest Damage Records).

California Interceptions: None reported.

The risk Phytophthora cambivora would pose to California is evaluated below.

Consequences of Introduction:

1) Climate/Host Interaction: Phytophthora cambivora has already established a large distribution under moist and cool to warm climates in California.

Evaluate if the pest would have suitable hosts and climate to establish in California.

Score: 2

– Low (1) Not likely to establish in California; or likely to establish in very limited areas.

– Medium (2) may be able to establish in a larger but limited part of California.

– High (3) likely to establish a widespread distribution in California.

2) Known Pest Host Range: The pathogen has a wide host range.

Evaluate the host range of the pest.

Score: 3

– Low (1) has a very limited host range.

– Medium (2) has a moderate host range.

– High (3) has a wide host range.

3) Pest Dispersal Potential: Phytophthora cambivora, like other Phytophthora, has high reproductive capability under moist conditions. It is dependent on moisture for spore dissemination and plant infection. It is soilborne and may be spread to non-infected sites through infected plants, nursery and planting stock, and seedlings, soil, run-off and splash irrigation and rain water, and contaminated cultivation equipment, tools, boots, rivers, canals, and ponds. Therefore, it is given a high rating in this category.

Evaluate the natural and artificial dispersal potential of the pest.

Score: 3

– Low (1) does not have high reproductive or dispersal potential.

– Medium (2) has either high reproductive or dispersal potential.

– High (3) has both high reproduction and dispersal potential.

4) Economic Impact: Damage caused by Phytophthora cambivora alone may be difficult to assess as more than one species of Phytophthora may be associated with root and crown rot of host tree. Loss in production has been reported for apple, certain stone fruit, and noble fir Christmas. Nursery productions of agricultural and environmental host planting stock, could be at risk. Controlling the disease include soil water management and use of resistant varieties, thereby requiring changes in cultural practices and increase in crop production costs.

Evaluate the economic impact of the pest to California using the criteria below.

Economic Impact: A, B, D, G

A. The pest could lower crop yield.

B. The pest could lower crop value (includes increasing crop production costs).

C. The pest could trigger the loss of markets (includes quarantines).

D. The pest could negatively change normal cultural practices.

E. The pest can vector, or is vectored, by another pestiferous organism.

F. The organism is injurious or poisonous to agriculturally important animals.

G. The organism can interfere with the delivery or supply of water for agricultural uses.

Economic Impact Score: 3

– Low (1) causes 0 or 1 of these impacts.

– Medium (2) causes 2 of these impacts.

– High (3) causes 3 or more of these impacts.

5) Environmental Impact: In conjunction with other Phytophthora, P. cambivora may be a contributor to root and crown disease of environmental plants. California’s native vegetation is at risk of root and crown rot damage caused by P. cambivora and other Phytophthora spp., many of which are endemic (limited) to the State, while some are rare, endangered, or threatened plants. The pathogen is capable of becoming established in a variety of native plant habitats under a range of soil and environmental conditions and can have negative impacts on native vegetation. Also, it may significantly impact ornamental planting.

Evaluate the environmental impact of the pest on California using the criteria below.

Environmental Impact: A, B, C, E

A. The pest could have a significant environmental impact such as lowering biodiversity, disrupting natural communities, or changing ecosystem processes.

B. The pest could directly affect threatened or endangered species.

C. The pest could impact threatened or endangered species by disrupting critical habitats.

D. The pest could trigger additional official or private treatment programs.

E. The pest significantly impacts cultural practices, home/urban gardening or ornamental plantings.

Environmental Impact Score: 3

– Low (1) causes none of the above to occur.

– Medium (2) causes one of the above to occur.

– High (3) causes two or more of the above to occur.

**Consequences of Introduction to California for Phytophthora cambivora:**

Add up the total score and include it here. 14

-Low = 5-8 points

-Medium = 9-12 points

–High = 13-15 points

6) Post Entry Distribution and Survey Information: Evaluate the known distribution in California. Only official records identified by a taxonomic expert and supported by voucher specimens deposited in natural history collections should be considered. Pest incursions that have been eradicated, are under eradication, or have been delimited with no further detections should not be included.

Evaluation is Score: (-3)

-Not established (0) Pest never detected in California, or known only from incursions.

-Low (-1) Pest has a localized distribution in California, or is established in one suitable climate/host area (region).

-Medium (-2) Pest is widespread in California but not fully established in the endangered area, or pest established in two contiguous suitable climate/host areas.

–High (-3) Pest has fully established in the endangered area, or pest is reported in more than two contiguous or non-contiguous suitable climate/host areas.

Final Score:

7) The final score is the consequences of introduction score minus the post entry distribution and survey information score: (Score)

Final Score: Score of Consequences of Introduction – Score of Post Entry Distribution and Survey Information = 11

Uncertainty:

None.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for Phytophthora cambivora is B.

References:

Adaskaveg, J. E., J. L. Caprile, W. D. Gubler, B. L. Teviotdale. 2009. Cherry: Phytophthora root and crown rot, pathogen: Phytophthora spp. UCIPM Statewide Integrated Pest Management Program, University of California Agriculture & Natural Resources. http://ipm.ucanr.edu/PMG/r105100711.html

Browne, G. T., and S. M. Mircetich. 1995. Phytophthora root and crown rots. In Compendium of Stone Fruit Diseases, Eds: J. M. Ogawa, E. I. Zehr, G. W. Bird, D. F. Ritchie, K. Uriu, and J. K. Uyemoto. APS Press, The American Phytopathological Society. Pages 38-40.

CABI. 2017. Phytophthora cambivora (root rot of forest trees) full datasheet. Crop Protection Compendium. http://www.cabi.org/cpc/datasheet/40956

Calflora. 2017. Information on California plants for education, research and conservation. [Web application]. 2017. Berkeley, California. The Calflora Database [a non-profit organization]. http://www.calflora.org/

CNPS. 2017. Inventory of rare and endangered plants of California (online edition, v8-03 0.38). California Native Plant Society, Rare Plant Program. Website http://www.rareplants.cnps.org [accessed 10 August 2017].

Cox, K. 2014. Phytophthora collar, crown, and root rots. In Compendium of Apple and Pear Disease and Pests Second Edition Eds: T. B. Sutton, H. S. Aldwinckle, A. M. Agnello, J. F. Walgenbach. Pages 63-65.

Farr, D. F., and A. Y. Rossman. 2017. Fungal Databases, U.S. National Fungus Collections, ARS, USDA. Retrieved June 9, 2017, from https://nt.ars-grin.gov/fungaldatabases/

French, A.M. 1989. California Plant Disease Host Index. California Department of Food and Agriculture, Sacramento (Updated online version by T. Tidwell, May 2, 2017).

Jung, T., M. H. Jung, B. Scanu, D. Seress, G. M. Kovács, C. Maia, A. Pérez-Aierra, T. –T. Chang, A. Chandelier, K. Heungens, K. van Poucke, P. Abad-Campos, M. Leon, S. O. Caciola, and J. Bakonyi. 2016. Six new Phytophthora species from ITS Clade 7a including two sexually functional heterothallic hybrid species detected in natural ecosystems in Taiwan. Persoonia 38: 100-135.

Mircetich, S. M., and M. E. Matherton. 1976. Phytophthora root and crown rot of cherry trees. Phytopathology 66: 549-558.

Saavedra, A., E. M. Hansen, and D. J. Goheen. 2007. Phytophthora cambivora in Oregon and its pathogenicity to Chrysolepis chrysophylla. Forest Pathology, 37: 409-419.

USDA PCIT. 2017. USDA Phytosanitary Certificate Issuance & Tracking System. Retrieved June 6, 2017. 5:59:40 pm CDT. https://pcit.aphis.usda.gov/PExD/faces/ReportHarmOrgs.jsp.

Responsible Party:

John J. Chitambar, Primary Plant Pathologist/Nematologist, California Department of Food and Agriculture, 3294 Meadowview Road, Sacramento, CA 95832. Phone: 916-262-1110, plant.health[@]cdfa.ca.gov.

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