Phytophthora pathogens threaten rare habitats and conservation plantings
DOI:
https://doi.org/10.24823/Sibbaldia.2020.288Abstract
Phytophthora pathogens are damaging native wildland vegetation including plants in restoration areas and botanic gardens. The infestations threaten some plants already designated as endangered and degrade high-value habitats. Pathogens are being introduced primarily via container plant nursery stock and, once established, they can spread to adjacent areas where plant species not previously exposed to pathogens may become infected. We review epidemics in California – caused by the sudden oak death pathogen Phytophthora
ramorum Werres, De Cock & Man in ‘t Veld and the first USA detections of P. tentaculata Kröber & Marwitz, which occurred in native plant nurseries and restoration areas – as examples to illustrate these threats to conservation plantings.
References
S., MCROBERTS, N. & THOMAS, C.
(2016). Detection of Phytophthora ramorum in
nurseries and forest lands in California in 2004 to
2009. Plant Disease, 100(1): 139–148.
BOURRET, T.B. (2018). Efforts to detect exotic
Phytophthora species reveal unexpected diversity.
PhD dissertation. University of California, Davis.
BOWCUTT, F. (2015). The Tanoak Tree: An
Environmental History of a Pacific Coast Hardwood.
University of Washington Press, Seattle, WA.
BRASIER, C.M., KIRK, S., DELCAN, J., COOKE,
D.E., JUNG, T. & MAN IN ’T VELD, W.A. (2004).
Phytophthora alni sp. nov. and its variants:
designation of emerging heteroploid hybrid
pathogens spreading on Alnus trees. Mycological
Research, 108(10): 1172–1184.
CALFLORA (WEB APPLICATION) (2019). Berkeley,
CA. Available online: https://www.calflora.org/
(accessed August 2019).
CALIFORNIA OAK MORTALITY TASK
FORCE (2017). November newsletter.
Available online: www.suddenoakdeath.org/
wp-content/uploads/2017/11/COMTF-Report-
November-2017-4.pdf (accessed April 2019).
CALIFORNIA OAK MORTALITY TASK FORCE
(2018). November newsletter. Available
online: www.suddenoakdeath.org/wp-content/
uploads/2018/11/COMTF-Report-Nov-2018.pdf
(accessed April 2019).
COBB, R., HARTSOUGH, P., ROSS, N., KLEIN, J.,
LAFEVER, D., FRANKEL, S. & RIZZO, D. (2017).
Resiliency or restoration: management of sudden
oak death before and after outbreak. Forest
Phytophthoras, 7(1): 1–14.
DAVIDSON, J.M., WICKLAND, A.C., PATTERSON,
H.A., FALK, K.R. & RIZZO, D.M. (2005).
Transmission of Phytophthora ramorum in mixedevergreen
forest in California. Phytopathology,
95(5): 587–596.
EAST BAY REGIONAL PARK DISTRICT (2017).
Pallid manzanita management plan, May 2017.
EYRE, C.A., KOZANITAS, M. & GARBELOTTO,
M. (2013). Population dynamics of aerial and
terrestrial populations of Phytophthora ramorum
in a California forest under different climatic
conditions. Phytopathology, 103(11): 1141–1152.
FRANKEL, S.J. (2008). Sudden oak death and
Phytophthora ramorum in the USA: a management
challenge. Australasian Plant Pathology, 37(1):
19–25.
FRANKEL, S.J., ALEXANDER, J., BENNER, D.
& SHOR, A. (2018). Coordinated response to
inadvertent introduction of pathogens to California
restoration areas. California Agriculture, 72(4):
205–207.
FRANKEL, S.J., SWIECKI, T.J., BERNHARDT, E.A.,
BENNER, D., BLOMQUIST, C. & ROONEY-LATHAM,
S. (2019). Accreditation to improve restoration
program shows promise for pathogen prevention.
Abstract. Seventh Sudden Oak Death Science and
Management Symposium, 25–27 June 2019, San
Francisco, CA.
FRANKEL, S.J., SWIECKI, T.J., BERNHARDT, E.A.,
BLOMQUIST, C. & ROONEY-LATHAM, S. (2015).
Pest Alert, Phytophthora tentaculata. USDA Forest
62 | Susan J. Frankel, Janice Alexander, Diana Benner, Janell Hillman & Alisa Shor
Service, Pacific Southwest Research Station.
Available online: http://www.suddenoakdeath.org/
wp-content/uploads/2015/02/P.tentaculata.Pest_.
Alert_.022315.pdf (accessed April 2019).
GARBELOTTO, M., FRANKEL, S.J. & SCANU, B.
(2018). Soil- and waterborne Phytophthora species
linked to recent outbreaks in northern California
restoration sites. California Agriculture, 72(4):
208–216.
GARBELOTTO, M. & HAYDEN, K.J. (2012). Sudden
oak death: interactions of the exotic oomycete
Phytophthora ramorum with naïve North American
hosts. Eukaryotic Cell, 11(11): 1313–1323.
GOHEEN, E.M., HANSEN, E.M., KANASKIE,
A., MCWILLIAMS, M.G., OSTERBAUER, N. &
SUTTON, W. (2002). Sudden oak death caused by
Phytophthora ramorum in Oregon. Plant Disease,
86(4): 441.
GOHEEN, E.M., KANASKIE, A., NAVARRO,
S. & HANSEN, E. (2017). Sudden oak death
management in Oregon tanoak forests. Forest
Phytophthoras, 7(1): 45–53.
GRÜNWALD, N.J., GARBELOTTO, M., GOSS,
E.M., HEUNGENS, K. & PROSPERO, S. (2012).
Emergence of the sudden oak death pathogen
Phytophthora ramorum. Trends in Microbiology,
20(3): 131–138.
GRÜNWALD, N.J., GOSS, E.M. & PRESS, C.M.
(2008). Phytophthora ramorum: a pathogen with
a remarkably wide host range causing sudden
oak death on oaks and ramorum blight on woody
ornamentals. Molecular Plant Pathology, 9(6):
729–740.
GRÜNWALD, N.J., LARSEN, M.M., KAMVAR, Z.N.,
REESER, P.W., KANASKIE, A., LAINE, J. & WIESE,
R. (2016). First report of the EU1 clonal lineage
of Phytophthora ramorum on tanoak in an Oregon
forest. Plant Disease, 100(5): 1024.
GRÜNWALD, N.J., LEBOLDUS, J.M. & HAMELIN,
R.C. (2019). Ecology and evolution of the sudden
oak death pathogen Phytophthora ramorum.
Annual Review of Phytopathology, 57. Review in
Advance. Available online: https://doi.org/10.1146/
annurev-phyto- 082718-100117 (accessed August
2019).
HAMMOND, M. (2018). Phytophthora impacts
to endangered pallid manzanita in the East Bay
Regional Park District. Abstract. 2018 California
Invasive Plant Council Symposium, 7–10 November,
2018, Monterey, CA.
HANSEN, E.M. (2007). Alien forest pathogens:
Phytophthora species are changing world forests.
Boreal Environment Research, 13: 33–41.
HANSEN, E.M. (2011). Phytophthora lateralis.
Forest Phytophthoras 1(1). Available online: http://
journals.oregondigital.org/ForestPhytophthora/
article/view/1816 (accessed April 2019).
HANSEN, E.M., KANASKIE, A., PROSPERO, S.,
MCWILLIAMS, M., GOHEEN, E.M., OSTERBAUER,
N., REESER, P. & SUTTON, W. (2008).
Epidemiology of Phytophthora ramorum in Oregon
tanoak forests. Canadian Journal of Forest Research,
38(5): 1133–1143.
HIGHLAND ECONOMICS, MASON, BRUCE &
GIRARD (2019). Sudden oak death: economic
impact assessment. Prepared for the Oregon
Department of Forestry. Salem, OR. Available
online: https://www.oregon.gov/ODF/Documents/
ForestBenefits/sudden-oak-death-economicimpact-
assessment.pdf (accessed April 2019).
HILLMAN, J., SWIECKI, T.J., BERNHARDT, E.A.,
MEHL, H.K., BOURRET, T.B. & RIZZO, D. (2017). 31
flavors to 50 shades of grey: Battling Phytophthoras
in native habitats managed by the Santa Clara
Valley Water District. In: FRANKEL, S.J. & HARRELL,
K.M. (tech. coords), Proceedings of the Sudden
Oak Death Sixth Science Symposium. Gen. Tech.
Rep. GTR-PSW-255. Albany, CA: U.S. Department
of Agriculture, Forest Service, Pacific Southwest
Research Station, p. 57.
HOLLORAN, P. (1996). The greening of the Golden
Gate: community-based restoration at the Presidio
of San Francisco. Restoration & Management Notes,
14(2): 112–123.
JUNG, T., ORLIKOWSKI, L., HENRICOT, B.,
ABAD-CAMPOS, P., ADAY, A.G., AGUÍN CASAL,
O., BAKONYI, J., CACCIOLA, S.O., CECH, T.,
CHAVARRIAGA, D., CORCOBADO, T., CRAVADOR,
A. 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., PÉREZ-SIERRA, A., DURÁN, A., HORTA,
M.J., BALCI, Y. & SCANU, B. (2018). Canker and
decline diseases caused by soil- and airborne
Phytophthora species in forests and woodlands.
Phytophthora pathogens threaten rare habitats and conservation plantings | 63
Persoonia: Molecular Phylogeny and Evolution of
Fungi, 40: 182–220.
KANASKIE, A. & NAVARRO, S. (2019).
Intensification of sudden oak death in Oregon
forests in the absence of eradication treatments.
Abstract. Seventh Sudden Oak Death Science and
Management Symposium, 25–27 June 2019, San
Francisco, CA.
KANASKIE, A., WIESE, R., NORLANDER, D., LAINE,
J., NAVARRO, S., GOHEEN, E.M., RHATIGAN,
R., HANSEN, E., SUTTON, W., REESER, P.,
GRÜNWALD, N., KAMVAR, Z. & OSTERBAUER,
N. (2017). Slowing spread of sudden oak death
in Oregon forests, 2001–2015. In: FRANKEL, S.J.
& HARRELL, K.M. (tech. coords), Proceedings of
the Sudden Oak Death Sixth Science Symposium.
Gen. Tech. Rep. GTR-PSW-255. Albany, CA: US
Department of Agriculture, Forest Service, Pacific
Southwest Research Station, p. 1.
KNAUS, B.J., FIELAND, V.J., GRAHAM, K.A. &
GRÜNWALD, N.J. (2015). Diversity of foliar
Phytophthora species on Rhododendron in Oregon
nurseries. Plant Disease, 99(10): 1326–1332.
LIEBHOLD, A.M., BROCKERHOFF, E.G., GARRETT,
L.J., PARKE, J.L. & BRITTON, K.O. (2012). Live
plant imports: the major pathway for forest insect
and pathogen invasions of the US. Frontiers in
Ecology and the Environment, 10: 135–143.
LYMAN, G., APPEL, J., INGOLIA, M., NATESAN, E.
& ORTIZ, J. (2017). Steam, solarization, and tons
of prevention: The San Francisco Public Utilities
Commission’s fight to contain Phytophthoras in San
Francisco Bay Area restoration sites. In: FRANKEL,
S.J. & HARRELL, K.M. (tech. coords), Proceedings of
the Sudden Oak Death Sixth Science Symposium.
Gen. Tech. Rep. GTR-PSW-255. Albany, CA: U.S.
Department of Agriculture, Forest Service, Pacific
Southwest Research Station, p. 56.
MASCHERETTI, S., CROUCHER, P.J.P., VETTRAINO,
A., PROSPERO, S. & GARBELOTTO, M. (2008).
Reconstruction of the sudden oak death epidemic
in California through microsatellite analysis of
the pathogen Phytophthora ramorum. Molecular
Ecology, 17(11): 2755-2768.
METZ, M., VARNER, J.M., MEENTEMEYER, R.,
FRANGIOSO, K. & RIZZO, D. (2017). Lessons from
15 years of monitoring sudden oak death and
forest dynamics in California forests. In: FRANKEL,
S.J. & HARRELL, K.M. (tech. coords), Proceedings of
the Sudden Oak Death Sixth Science Symposium.
Gen. Tech. Rep. GTR-PSW-255. Albany, CA: US
Department of Agriculture, Forest Service, Pacific
Southwest Research Station, pp. 2–3.
MOUNCE, R., SMITH, P. & BROCKINGTON, S.
(2017). Ex situ conservation of plant diversity
in the world’s botanic gardens. Nature Plants, 3:
795–802.
NATIONAL PARK SERVICE (undated). Raven’s
Manzanita. Available online: https://www.nps.gov/
prsf/learn/nature/ravens-manzanita.htm (accessed
April 2019).
NAVARRO, S., WIESE, R., NICHOLS, C.,
NORLANDER, D., KANASKIE, K., GOHEEN,
E.M., HANSEN, E., SUTTON, W., REESER, P.,
GRÜNWALD, N. & LEBOLDUS, J. (2019). Slowing
the spread of sudden oak death in Oregon forests,
2001-2018. Abstract. Seventh Sudden Oak Death
Science and Management Symposium, 25–27 June
2019, San Francisco, CA.
OREGON DEPARTMENT OF AGRICULTURE (2001).
Phytophthora ramorum quarantine, 603-052-1230;
Phytophthora ramorum Regulated Area for Nursery
Stock, 603-052-1250. Plant Health Quarantines and
Control Area Orders. Available online: https://www.
oregon.gov/ODA/programs/PlantHealth/Pages/
PlantHealthQuarantines.aspx (accessed April 2019).
PARKE, J.L., KNAUS, B.J., FIELAND, V.J., LEWIS,
C. & GRÜNWALD, N.J. (2014). Phytophthora
community structure analyses in Oregon
nurseries inform systems approaches to disease
management. Phytopathology, 104: 1052–1062.
PÉREZ-SIERRA, A. & JUNG, T. (2013).
Phytophthora in woody ornamental nurseries.
In: LAMOUR, K. (ed.), Phytophthora: A Global
Perspective. CABI, Plant Protection Series 2. CABI,
London, pp. 166–177.
PERRING, M.P., STANDISH, R.J., PRICE, J.N.,
CRAIG, M.D., ERICKSON, T.E., RUTHROF, K.X.,
WHITELEY, A.S., VALENTINE, L.E. & HOBBS, R.J.
(2015). Advances in restoration ecology: rising to
the challenges of the coming decades. Ecosphere,
6(8): 131.
PETERSON, E.K., HANSEN, E.M. & KANASKIE, A.
(2015). Temporal epidemiology of sudden oak
death in Oregon. Phytopathology, 105(7): 937–946.
PHYTOPHTHORAS IN NATIVE HABITATS
WORK GROUP (2016). Guidelines to minimize
64 | Susan J. Frankel, Janice Alexander, Diana Benner, Janell Hillman & Alisa Shor
Phytophthora pathogens in restoration nurseries.
Available online: http://www.suddenoakdeath.org/
wp-content/uploads/2016/04/Restoration.Nsy_.
Guidelines.final_.092216.pdf (accessed April 2019).
REICHARD, S.H. & WHITE, P. (2001). Horticulture
as a pathway of invasive plant introductions in
the United States: most invasive plants have been
introduced for horticultural use by nurseries,
botanical gardens, and individuals. BioScience,
51(2): 103–113.
RIZZO, D.M., GARBELOTTO, M. & HANSEN,
E.M. (2005). Phytophthora ramorum: integrative
research and management of an emerging
pathogen in California and Oregon forests. Annual
Review of Phytopathology, 43: 309–335.
ROLSTON, H. (1985). Duties to endangered
species. BioScience, 35(11): 718–726.
ROONEY-LATHAM, S. & BLOMQUIST, C.L.
(2014). First report of root and stem rot caused by
Phytophthora tentaculata on Mimulus aurantiacus in
North America. Plant Disease, 98(7): 996.
ROONEY-LATHAM, S., BLOMQUIST, C.L.,
KOSTA, K.L., GOU, Y.Y. & WOODS, P.W. (2019).
Phytophthora species are common on nursery stock
grown for restoration and revegetation purposes in
California. Plant Disease, 103(3): 448–455.
ROONEY-LATHAM, S., BLOMQUIST, C.L.,
SWIECKI, T., BERNHARDT, E. & FRANKEL, S.J.
(2015). First detection in the US: New plant
pathogen, Phytophthora tentaculata, in native plant
nurseries and restoration sites in California. Native
Plants Journal, 16(1): 23–27.
ROONEY-LATHAM, S., BLOMQUIST, C.L.,
WILLIAMS, A., GUNNISON, E. & PASTALKA,
T. (2017). Identification of five new hosts of
Phytophthora ramorum in an infested forest in
California. In: FRANKEL, S.J. & HARRELL, K.M. (tech.
coords), Proceedings of the Sudden Oak Death Sixth
Science Symposium. Gen. Tech. Rep. GTR-PSW-255.
Albany, CA: US Department of Agriculture, Forest
Service, Pacific Southwest Research Station, pp.
83–84.
SCHWARTZBURG, K., HARTZOG, H., LANDRY,
C., ROGERS, J. & RANDALL-SCHADEL, B. (2009).
Prioritization of Phytophthora of concern to the
United States. USDA APHIS PPQ CPHST PERAL,
Raleigh, NC.
SCOTT, P. & WILLIAMS, N. (2014). Phytophthora
diseases in New Zealand forests. New Zealand
Journal of Forestry, 59(2): 14–21.
SEDDON, P.J., GRIFFITHS, C.J., SOORAE, P.S. &
ARMSTRONG, D.P. (2014). Reversing defaunation:
restoring species in a changing world. Science,
345(6195): 406–412.
SIMAMORA, A.V., PAAP, T., HOWARD, K.,
STUKELY, M.J., HARDY, G.E.S.J. & BURGESS,
T.I. (2018). Phytophthora contamination in a
nursery and its potential dispersal into the natural
environment. Plant Disease, 102(1): 132–139.
SIMS, L.L., CHEE, C., BOURRET, T., HUNTER, S. &
GARBELOTTO, M. (2019). Genetic and phenotypic
variation of Phytophthora crassamura isolates from
California nurseries and restoration sites. Fungal
Biology, 123(2): 159–169.
SIMS, L.L. & GARBELOTTO, M. (2018).
Susceptibility to the rare Phytophthora tentaculata
and to the widespread Phytophthora cactorum is
consistent with host ecology and history. Forest
Pathology, 48(5): e12446.
SIMS, L., TJOSVOLD, S., CHAMBERS, D. &
GARBELOTTO, M. (2019). Control of Phytophthora
species in plant stock for habitat restoration
through best management practices. Plant
Pathology, 68(1): 196–204.
SWIECKI, T.J., BERNHARDT, E.A. & FRANKEL,
S.J. (2018a). Phytophthora root disease and the
need for clean nursery stock in urban forests. Part
1. Phytophthora invasions in the urban forest and
beyond. Western Arborist, 44(3): 54–60.
SWIECKI, T.J., BERNHARDT, E.A. & FRANKEL, S.J.
(2018b). Phytophthora root disease and the need
for clean nursery stock in urban forests. Part 2.
Phytophthora in nurseries. Western Arborist, 44(4):
38–45.
SWIECKI, T.J., BERNHARDT, E.A. & FRANKEL, S.J.
(2019). Phytophthora root disease and the need
for clean nursery stock in urban forests: Part 3.
Prevention and management. Western Arborist,
45(1): 40–50.
US DEPARTMENT OF AGRICULTURE (2002). Code
of Federal Regulations 301.92 Title 7 – Restrictions
on interstate movement. Domestic quarantine
notices. Phytophthora ramorum. Available online:
https://www.govinfo.gov/content/pkg/CFR-2018-
title7-vol5/xml/CFR-2018-title7-vol5-sec301-92.xml
(accessed April 2019).
Phytophthora pathogens threaten rare habitats and conservation plantings | 65
US DEPARTMENT OF AGRICULTURE (2013).
List of regulated hosts and plants associated
with Phytophthora ramorum. US Department of
Agriculture, Animal and Plant Health Inspection
Service. August 2013. Available online: https://
www.aphis.usda.gov/plant_health/plant_pest_
info/pram/downloads/pdf_files/usdaprlist.pdf
(accessed April 2019).
US FISH AND WILDLIFE SERVICE (1998).
Endangered and threatened wildlife and plants:
Determination of threatened status for one plant,
Arctostaphylos pallida (Pallid Manzanita), From
the Northern Diablo Range of California. Federal
Register, 63(77): 19842–19850.
VALACHOVIC, Y., TWIEG, B., LEE, C., COBB, R. &
STARK, D. (2017). Forest stand conditions after
Phytophthora ramorum management in northern
California: post-treatment observations inform
future responses. Forest Phytophthoras 7(1): 54–66.
WEILAND, J.E., SCAGEL, C.F., GRÜNWALD,
N.J., DAVIS, E.A., BECK, B.R. & FIELAND, V.J.
(2018). Variation in disease severity caused by
Phytophthora cinnamomi, P. plurivora, and Pythium
cryptoirregulare on two Rhododendron cultivars.
Plant Disease, 102(12): 2560–2570.
YAKABE, L.E., BLOMQUIST, C.L., THOMAS, S.L.
& MACDONALD, J.D. (2009). Identification and
frequency of Phytophthora species associated with
foliar diseases in California ornamental nurseries.
Plant Disease, 93(9): 883–890.
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