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Phytophthora Pathogens Threaten Rare Habitats and Conservation Plantings

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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 frst USA detections of P. tentaculata Krber & 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 identifed 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 frst discovered in California 1 Susan J. Frankel is a Plant Pathologist with the USDA Forest Service. Address: Pacifc 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 frst Wildland and restoration detections in the USA of P. tentaculata Phytophthora epidemics in Krber & 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 densiforus (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 difcult 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 (Grnwald et al., 2008; Grnwald 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. beneft. 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. Eforts to 1998) or threatened species (Calfora, 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 efects 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 frst 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 Scientifc 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,
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