Phytophthora Pathogens Threaten Rare Habitats and Conservation Plantings

Phytophthora pathogens threaten rare habitats and conservation plantings

Susan J. Frankel1, Janice Alexander2, Diana Benner3, Janell Hillman4 & Alisa Shor5

Abstract 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.

Introduction stock) (Liebhold et al., 2012; Parke et al., Phytophthora (order: Peronosporales; 2014; Jung et al., 2015; Swiecki et al., kingdom: Stramenopila) pathogens 2018b; Sims et al., 2019). Once established, have increasingly been identified as Phytophthora spp. have the potential associated with plant dieback and to reduce growth, kill and cause other mortality in restoration areas (Bourret, undesirable impacts on a wide variety of 2018; Garbelotto et al., 2018; Sims et al., native or horticultural vegetation (Brasier 2019), threatened and endangered species et al., 2004; Hansen 2007, 2011; Scott & habitat (Swiecki et al., 2018a), botanic Williams, 2014; Jung et al., 2018). gardens and wildlands in coastal California In this review, we focus on the (Cobb et al., 2017; Metz et al., 2017) and consequences of two pathogen southern Oregon (Goheen et al., 2017). introductions: the sudden oak death The pathways for Phytophthora and other pathogen Phytophthora ramorum Werres, pathogen introductions are not always De Cock & Man in ‘t Veld, as it attacks known but often they arrive inadvertently new host species more than two decades on infested plants for planting (nursery after it was first discovered in California

1 Susan J. Frankel is a Plant Pathologist with the USDA Forest Service. Address: Pacific Southwest Research Station, 800 Buchanan Street, Albany, CA 94710, USA. Email: [email protected] 2 Janice Alexander is Outreach Specialist at University of California Cooperative Extension, Marin County. Address: 1682 Novato Blvd # 150B, Novato, CA 94947, USA. 3 Diana Benner is owner of the Watershed Nursery. Address: 601 A Canal Blvd, Richmond, CA 94804, USA. 4 Janell Hillman is Senior Biologist/Plant Ecologist at Santa Clara Valley Water District. Address: 5750 Almaden Expressway, San Jose, CA 95118, USA. 5 Alisa Shor is Director of Park Nurseries, Golden Gate National Parks Conservancy. Address: 201 Fort Mason, San Francisco, CA 94123, USA. 54 | Susan J. Frankel, Janice Alexander, Diana Benner, Janell Hillman & Alisa Shor

(Rooney-Latham et al., 2017), and the first Wildland and restoration detections in the USA of P. tentaculata Phytophthora epidemics in Kröber & Marwitz, which occurred in California California native plant nurseries and The sudden oak death pathogen restoration plantings from 2012 to 2014 spreads from wildlands to rare (Rooney-Latham et al., 2015; Sims et al., plants 2018). For more than 30 years, coastal California Follow-up investigations of these and Oregon landscapes have been under epidemics revealed that Phytophthora attack by the invasive sudden oak death pathogens are common in ornamental pathogen, Phytophthora ramorum, where nurseries (Yakabe et al., 2009; Parke et al., over 50 million trees have been killed, 2014; Knaus et al., 2015; Blomquist et al., primarily Notholithocarpus densiflorus (Hook. 2016) and, in California, native plant nurseries & Arn.) Manos, Cannon & S.H. Oh (tanoak) and are being introduced to new areas and Quercus agrifolia Née (coast live oak) when outplanted (Sims et al., 2018; Rooney- (Rizzo et al., 2005; Frankel, 2008; Garbelotto Latham et al., 2019; Swiecki et al., 2019). Once & Hayden, 2012; California Oak Mortality Task established, Phytophthora pathogens may Force (COMTF), 2018) (Fig. 1). The pathogen infest the site and often are very difficult has been introduced several times, most to eradicate or curtail (Goheen et al., 2017; likely on ornamental nursery stock; once Valachovic et al., 2017). established, it spread via windblown rain We focus on invasions into conservation into adjacent forests, parks and gardens or mitigation plantings, such as rare plant (Grünwald et al., 2008; Grünwald et al., 2012). habitats, botanic gardens or restoration Unexpectedly, starting in 2015 after two areas. Since these plantings are designed decades of monitoring, several more plant to improve habitats, enhance biodiversity species, including Chrysolepis chrysophylla or expand plant populations with high (Douglas ex Hook.) Hjelmqvist (chinquapin), conservation value, their failure degrades Pickeringia montana Nutt. ex Torr. & A. Gray the natural resources that they aim to (chaparral pea) and rare Arctostaphylos spp. benefit. Taken together, these California Adans. (manzanitas) were recognised as plant pathogen introductions serve as hosts showing symptoms of dieback and evidence that without additional preventive mortality (COMTF, 2017; Rooney-Latham measures to ensure nursery stock health, et al., 2017). Many of these plant hosts are actions intended to sustain and protect endangered (US Fish and Wildlife Service, species may be undermined. Efforts to 1998) or threatened species (Calflora, 2019) retain remnant plant populations in botanic and several of the invasions occurred in gardens or restoration areas can be destroyed botanic garden collections. These detections if measures are not taken to ensure that demonstrate the detrimental effects that plant pathogens are not introduced into invasive pathogens can have on plant life. P. rare habitats, or elsewhere, where they ramorum is known to infect over 100 plant can eventually encroach into conservation species including hardwoods, conifers, plantings. shrubs, herbaceous plants and ferns (US Department of Agriculture, 2013). Its broad Phytophthora pathogens threaten rare habitats and conservation plantings | 55 host range includes common plants, such as manzanita), A. montereyensis Hoover (Toro tanoak (Bowcutt, 2015), and, over time, rare manzanita), A. morroensis Wiesl. & Schreiber plants in conservation plantings and remnant (Morro manzanita), A. pilosula Jeps. & Wiesl. habitats have been found as symptomatic (La Panza manzanita), A. pumila Nutt. (dune and infected, apparently exposed to inoculum manzanita) and A. silvicola Jeps. (Bonny from nearby infested forests (Davidson et al., Doon manzanita) (Matteo Garbelotto, pers. 2005; Hansen et al., 2008). comm.). The pathogen was also reported on From 2015 to 2017, Phytophthora multiple rare manzanita species at the East ramorum was first recognised on several Bay Regional Park Botanic Garden in Tilden rare, threatened or endangered manzanita Park near Berkeley, CA (Alameda County) species in wildlands and botanic gardens – further details will be published soon (Table 1). In maritime chaparral of Marin by the California Department of Food and and San Mateo Counties infection was Agriculture (Suzanne Rooney-Latham, CDFA, observed on Arctostaphylos glandulosa Eastw. pers. comm.). Symptoms appeared as leaf (Eastwood manzanita), A. virgata Eastw. spots, dieback or complete plant mortality. All (Marin manzanita) (Rooney-Latham et al., the detections occurred in areas known to be 2017) and A. montaraensis Roof (Montara infested with P. ramorum for several decades, manzanita) (Matteo Garbelotto, University but symptoms on manzanita species had not of California, Berkeley, pers. comm.). previously been reported. Additionally, the pathogen infested plants Also on East Bay Regional Park District in two botanic gardens. In the University of (EBRPD) lands, Phytophthora ramorum was California, Santa Cruz Arboretum and Botanic found damaging Arctostaphylos pallida Garden (Santa Cruz County), P. ramorum was Eastw. (pallid manzanita), a state endangered detected on A. hooveri P.V. Wells (Hoover’s plant. State law requires the EBRPD protect

Fig. 1 Sudden oak death of tanoak in Sonoma County, CA. Photo: Christopher Lee, California Department of Forestry and Fire Protection. 56 | Susan J. Frankel, Janice Alexander, Diana Benner, Janell Hillman & Alisa Shor

Scientific name Location, Year Reference Arctostaphylos Wildland, Marin Co., 2015 Rooney-Latham et al., 2017 glandulosa Arctostaphylos Botanic Garden, Santa Cruz Co., Matteo Garbelotto, University of hooveri 2017 California, Berkeley, pers. comm. Arctostaphylos Wildland, San Mateo Co., 2017 Matteo Garbelotto, University of montaraensis California, Berkeley, pers. comm. Discovered in 2017 SOD Blitz survey. Arctostaphylos Botanic Garden, Santa Cruz Co., Matteo Garbelotto, University of montereyensis 2017 California, Berkeley, pers. comm. Arctostaphylos Botanic Garden, Santa Cruz Co., Matteo Garbelotto, University of morroensis 2017 California, Berkeley, pers. comm. Arctostaphylos Wildland, Alameda Co., 2017 Swiecki et al., 2018a pallida Arctostaphylos Botanic Garden, Santa Cruz Co., Matteo Garbelotto, University of pilosula 2017 California, Berkeley, pers. comm. Arctostaphylos Botanic Garden, Santa Cruz Co., Matteo Garbelotto, University of pumila 2017 California, Berkeley, pers. comm. Arctostaphylos Botanic Garden, Santa Cruz Co., Matteo Garbelotto, University of silvicola 2017 California, Berkeley, pers. comm. Arctostaphylos Wildland, Marin Co., 2015 Rooney-Latham et al., 2017 virgata

Table 1 Partial list of Arctostaphylos spp. (manzanitas) showing symptoms of P. ramorum infection discovered in California since 2015. All the plants developed symptoms in natural conditions.

A. pallida populations while the EBRPD introduced again in 2008 and 2014 (Grünwald manages this maritime chaparral habitat in et al., 2016; Goheen et al., 2017). An the wildland-urban interface for plant health interagency team conducted early detection and fire fuels management. In response, monitoring and mandatory eradication from botanists and plant pathologists have 2001 to 2012, which slowed but did not inventoried the populations, surveyed for stop pathogen spread and intensification pathogens, removed invasive weeds and (Peterson et al., 2015). As required by state deposited seed of pallid manzanita in several regulations, infested trees and other host banks (EBRPD, 2017; Hammond, 2018). plants were cut and burned along with a Oregon’s Phytophthora ramorum buffer of adjacent vegetation (Goheen et al., infestation demonstrates how difficult this 2017). From 2009 to 2011, funding limitations pathogen is to control in forests and that resulted in a treatment backlog of many introductions on nursery plants continue infestations near the centre of the quarantine despite quarantines. In Oregon, P. ramorum area (Kanaskie et al., 2017), which led to was first discovered in coastal south-west creation of a Generally Infested Area (GIA) Oregon forests in Curry County in July 2001 in which eradication was no longer required (Goheen et al., 2002) and subsequently by law (Kanaskie & Navarro, 2019). In the Phytophthora pathogens threaten rare habitats and conservation plantings | 57 absence of eradication treatments within Department of Agriculture, 2001) quarantines, the GIA, tanoak mortality increased rapidly another, more aggressive lineage of the (Fig. 2). Oregon Department of Forestry pathogen, the European Union 1 (EU1) clonal reports that on ten 1-ha plots near Brookings, lineage, was detected as introduced for the Oregon (Curry County), overstorey tanoak first time into a USA forest, on tanoak located mortality increased from less than 5 per cent approximately 1.6 km from a small private to an average of 87 per cent over a four-year nursery near the Pistol River (Curry County, period. Also from 2012 through 2017 the Oregon) (Grünwald et al., 2016; Grünwald disease spread rapidly, and the untreated, et al., 2019). The EU1 clonal lineage was infested area within the 151 sq. km GIA also found in the nursery (Grünwald et al., increased from 85 ha to more than 1,020 ha 2016). State-mandated eradication has been (Kanaskie & Navarro, 2019). conducted on over 190 ha that harboured the The threat of new Phytophthora ramorum EU1 lineage of P. ramorum, but the pathogen infestations from nursery stock movement continues to spread (Navarro et al., 2019). was demonstrated yet again in Oregon in The Sudden Oak Death: Economic 2015, where despite federal (7 CFR 301.92, US Assessment, conducted for the Oregon Department of Agriculture, 2002) and state Department of Forestry concluded that if the (603-052-1230 and 603-052-1250, Oregon current sudden oak death treatment regime

Fig. 2 Aerial view of mortality of dominant and co-dominant tanoaks killed by Phytophthora ramorum inside the Generally Infested Area near Brookings, OR. Photo: Oregon Department of Forestry. 58 | Susan J. Frankel, Janice Alexander, Diana Benner, Janell Hillman & Alisa Shor

(clear-cutting of infestations on the leading quantification, particularly tribal cultural edge of disease expansion) was terminated, values (Highland Economics et al., 2019). serious economic impacts might occur as Phytophthora ramorum moved north into Phytophthora tentaculata and Coos County (Highland Economics et al., other Phytophthora detections in 2019). Projected impacts included quarantines California restoration areas and on south-west Oregon timber exports by native plant nurseries China, Japan and Korea resulting in a loss of Over the past five years, Phytophthora species 1,200 jobs related to timber export, equal have been introduced into restoration areas to $57.9 million in annual wages, as well due to outplanting of infested nursery as other losses in revenue from depressed container plants (Garbelotto et al., 2018; property values and a decrease in tourism. Swiecki et al., 2018a, b; 2019). In 2012, P. The assessment also states that P. ramorum tentaculata was discovered causing severe strikes at core values that elude economic root and crown rot on Diplacus aurantiacus Jeps. (sticky monkey flower) at a native plant nursery in Monterey County and noted as a first USA detection (Rooney-Latham & Blomquist, 2014). In 2014, the pathogen was detected in five California native plant nurseries (Butte, Monterey, Placer, Santa Cruz Counties) and three habitat restoration sites in Monterey and Alameda Counties (Frankel et al., 2015) (Fig. 3). These detections shocked plant ecologists, as well as native plant growers, as evidence emerged that P. tentaculata had been unintentionally but extensively introduced into habitat restoration sites in the greater San Francisco Bay Area (Frankel et al., 2018; Garbelotto et al., 2018). Several habitat restoration sites designed to serve as mitigation for municipal water infrastructure projects were inadvertently planted with Phytophthora tentaculata infected plants including Frangula californica (Eschsch.) A. Gray (coffeeberry), Heteromeles arbutifolia (Lindl.) M. Roem. (toyon) and others (Fig. 4). The plantings extended along several kilometres of riparian area at various locations in Alameda County (Lyman et al., 2017) (Fig. 4). In another first Fig. 3 Phytophthora tentaculata infected Diplacus detection in the USA, P. quercina was found aurantiacus (sticky monkey flower) in a restoration planting in Alameda County, CA, in 2014. Photo: Tedmund on a planted Quercus lobata Née (valley oak) Swiecki, Phytosphere Research. in a restoration area in San Jose (Santa Clara Phytophthora pathogens threaten rare habitats and conservation plantings | 59

Fig. 4 Alameda County restoration site showing coloured flags noting locations of outplanted container nursery stock. Post-planting, the site tested positive for Phytophthora. Photo: Tedmund Swiecki, Phytosphere Research.

County) (Swiecki et al., 2018a). In 2009, Agriculture diagnostic lab for Phytophthora both P. quercina and P. tentaculata were testing. Phytophthora was confirmed from listed among the top five most threatening over three quarters (77 per cent) of the 26 Phytophthora species, not yet detected in the participating nurseries, on 37 per cent of USA, in an USDA Animal and Plant Health the 402 samples tested from plants in 22 Inspection Service (APHIS) pest risk analysis host families (Rooney-Latham et al., 2019). (Schwartzburg et al., 2009), so plant ecologists Rooney-Latham et al. (2019) conclude that were challenged with developing a means to their findings “document the widespread contain these infestations. occurrence of Phytophthora spp. in native In response to these soil-borne plant nurseries and highlight the potential Phytophthora introductions, project managers risks associated with outplanting infested suspended plantings, cancelled orders nursery-grown stock into residential gardens of nursery stock and invested millions of and wildlands”. dollars in solarisation treatments to clean In 2015, recognising that neither up contaminated sites. But such measures discontinuation of restoration planting nor achieved only partial eradication (Hillman et a switch to direct seeding represent an al., 2017; Lyman et al., 2017). The California ideal long-term approach to Phytophthora native plant nursery industry responded prevention, we created the Phytophthoras by voluntarily submitting samples to in Native Habitats Work Group (the Work the California Department of Food and Group)6 to develop best management

6 See www.calphytos.org 60 | Susan J. Frankel, Janice Alexander, Diana Benner, Janell Hillman & Alisa Shor

practices and other recommendations to evening primrose). The nursery is working prevent further pathogen introductions and to improve production practices to prevent ensure that the benefits of restoration are not future pathogen introductions. The virulence foregone or significantly delayed due to plant of P. pseudocryptogea on native plants is health risks. not fully known but it has been detected The Work Group utilises an on Arctostaphylos hookeri G. Don ssp. ravenii interdisciplinary, collaborative approach P.V. Wells (Raven’s manzanita) on federally to bring together native plant growers, managed lands of the Presidio (San Francisco, vegetation managers, restoration design CA). Raven’s manzanita is an endangered and installation contractors, regulators and species; in the mid-1980s only one single plant pathologists to address the potential plant existed (Rolston, 1985; Holloran, 1996). for pathogen introduction in all phases The plant has been cloned but some of the of restoration from design to planting clones are suffering significant dieback due to and site maintenance. The Work Group is Phytophthora infection as well as other pest currently conducting a pilot project, entitled problems (National Park Service, undated). “Accreditation to Improve Restoration and Native Plant Nursery Stock Cleanliness” (AIR), Conclusions to promote sanitation and other preventive Examining the consequences of these plant measures in restoration nurseries (Frankel pathogen epidemics demonstrates the et al., 2019; Swiecki et al., 2019). Eleven importance of prevention to avert pathogen California nurseries have voluntarily enrolled introductions to sustain and protect rare and committed to a self-assessment followed plants and habitats. Once introduced into by an external audit to confirm that they are landscapes, these pathogens are very producing plants with the practices outlined difficult to impossible to control (Kanaskie by the Work Group (2016) best management & Navarro, 2019) and may cause damage to practices for restoration nursery stock. These many high-value plants (Garbelotto et al., practices require growers to dedicate a 2018). When environmental conditions are significant amount of time and attention to favourable, pathogens may spread through phytosanitation throughout their operations. soil or water movement or via windblown rain The nursery assessment covers all aspects and colonise numerous plant species (Eyre et of nursery production, divided into 12 al., 2013). categories including layout, water source, Nurseries are widely distributed media, propagation and sanitation practices. throughout the US (Reichard et al., 2001) and To date, four nurseries have completed their irrigated conditions are conducive to all the requirements and have been deemed Phytophthora development (Swiecki et al., “AIR compliant”, valid for one year. However, 2018b). Nursery production poses a risk for in one of the participating nurseries in pathogen development and spread within Sonoma County, as part of the voluntary and beyond their facilities via contaminated inspection, auditors detected Phytophthora run-off or outplanted stock (Pérez-Sierra & pseudocryptogea Safaief., Mostowf., G.E. Hardy Jung, 2013; Simamora et al., 2018; Weiland et & T.I. Burgess infection on an endangered al., 2018). Best management practices that species, Oenothera deltoides Torr. & Frém. emphasise strict phytosanitation can prevent ssp. howellii (Munz) W. Klein (Antioch Dunes pathogen development in nurseries (Sims et Phytophthora pathogens threaten rare habitats and conservation plantings | 61 al., 2019), and thereby protect adjacent and CA. Available online: https://www.calflora.org/ distant natural areas. (accessed August 2019). Climate change and human population CALIFORNIA OAK MORTALITY TASK pressure are increasing the desire and need FORCE (2017). 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