Botany Expansion of the invasive European mistletoe in California, USA Journal: Botany Manuscript ID cjb-2019-0215.R1 Manuscript Type: Article Date Submitted by the 04-Feb-2020 Author: Complete List of Authors: Shaw, David ; Oregon State University, Department of Forest Engineering, Resources, and Management Lee, Christopher; California Department of Forestry and Fire Protection California, European mistletoe, introduction, invasive, Viscum Keyword: Draft album<i></i> Is the invited manuscript for consideration in a Special IUFRO 2019 Dwarf Mistletoes Symposium Issue? : https://mc06.manuscriptcentral.com/botany-pubs Page 1 of 26 Botany European mistletoe in California, USA 1 Expansion of the invasive European mistletoe in California, USA 2 3 David C. Shaw* 4 Department of Forest Engineering, Resources, and Management, Peavy Hall 5 Oregon State University, Corvallis, Oregon, USA. 6 [email protected] 7 8 Christopher A. Lee Draft 9 California Department of Forestry and Fire Protection 10 Fortuna, California, USA. [email protected] 11 12 *corresponding author: 13 David C. Shaw 14 Department of Forest Engineering, Resources, and Management 15 280 Peavy Hall 16 Oregon State University 17 Corvallis, Oregon, 97331, USA. 18 [email protected] 19 phone: 541.737.2845 20 fax: 541.737.4316 1 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 2 of 26 European mistletoe in California, USA 21 22 Abstract 23 The horticulturist Luther Burbank introduced the European mistletoe (Viscum album) to 24 Sebastopol, Sonoma County, California, USA around 1900 to grow as a Christmas ornament 25 crop and tincture for medicinal use. The mistletoe has since spread from the point of 26 introduction on apple to other hardwood trees, especially non-native hardwoods in yards and 27 farms of the region. Mistletoe surveys were previously conducted in 1971, 1986, and 1991. We 28 re-surveyed the region in 2019, with emphasis on the 1991 perimeter, and documented the 29 current farthest distribution of V. album. This represents a 120-year record of spread. We 30 observed infected trees up to 24.6 km (15.3Draft miles) from the point of introduction, doubling the 31 farthest distance reported in 1991. The estimated area encompassed by mistletoe-infected hosts 32 increased from 184 km2 (71 miles2) in 1991 to 606 km2 (234 miles2) in 2019. We also updated 33 the host species list including both native and non-native mistletoe hosts. Viscum album spread 34 appears to be limited by available habitat and hosts but within the survey area it is intensifying, 35 concentrated in urban and semi-urban yards, streets, and farms. However, V. album was also 36 commonly found in riparian areas, which have a large number of native hosts. 37 38 Keywords: California, European mistletoe, introduction, invasive, Viscum album 39 2 https://mc06.manuscriptcentral.com/botany-pubs Page 3 of 26 Botany European mistletoe in California, USA 40 Introduction 41 The European mistletoe (Viscum album L.) is widely distributed in Europe, but was 42 introduced into Sonoma County, CA by the horticulturist Luther Burbank in about 1900 (Sharpf 43 and Hawksworth 1976). This mistletoe is important as a parasite of orchard, plantation, and 44 urban hardwoods, yet it is also a significant economic crop, utilized as a Christmas ornament and 45 for medicinal purposes (Hawksworth 1983; Butin 1995; Mathiasen et al. 2008) (Fig. 1). It has the 46 largest host range of any mistletoe (Barney et al. 1998). Three common subspecies of Viscum 47 album L. are Viscum album subsp. album L. infects hardwoods in much of Europe, V. album 48 subsp. austriacum (Wiesb.) Vollmann is a parasite of pines (Pinus spp.), but occasionally infects 49 spruces (Picea spp.) and larches (Larix Draftspp.), and V. album subsp. abietis (Wiesb.) Abromeit 50 occurs only on true firs (Abies spp.) (Zuber 2004). Other subspecies of V. album may also occur 51 in Crete and Asia (Zuber 2004)). We believe the subspecies in Sonoma county is V. album 52 subsp. album because of its wide host range on dicotyledonous trees. European mistletoe may be 53 the most well-known and well-studied mistletoe in the world, particularly due to its use as a 54 Christmas ornament as well as for medicinal properties (Hawksworth 1983; Lev et al. 2011; 55 Freuding et al. 2019). The potential for commercialization of mistletoe is significant. 56 Around 1900, Luther Burbank, the horticulturist and Renaissance Man (Pandora 2001), 57 introduced the European mistletoe (subsp. album) to his experimental farm in Sebastopol, 58 California, apparently on an apple tree (Scharpf and McCartney 1975; Scharpf and Hawksworth 59 1976). It is believed he did this to develop the two crop applications mentioned above. However, 60 it was not until the detections and descriptions of McCartney (1968) and McCartney et al (1973) 61 that European mistletoe occurrence in California was documented. Then, in 1976, Scharpf and 62 Hawksworth went to unpublished notes of Luther Burbank and found that he propagated seed 3 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 4 of 26 European mistletoe in California, USA 63 supplied to him by a seed dealer in Chicago (Sharpf and Hawksworth 1976). The European 64 mistletoe has spread, becoming established in Sonoma County on multiple hosts (McCartney 65 1968; McCartney et al. 1973; Scharpf and McCartney 1975; Scharpf and Hawksworth 1976; 66 Hawksworth and Scharpf 1986; Hawksworth et al. 1991) (Fig. 2). European mistletoe was also 67 introduced into the Victoria, British Columbia, Canada area (Dorworth 1989) on apple, where it 68 has been eradicated (Kope in press). 69 From the 1960s-1980s, forest pathologists became alarmed at the potential for European 70 mistletoe to become a significant pest in California (McCartney 1968; McCartney et al. 1973; 71 Scharpf and McCartney 1975; Scharpf and Hawksworth 1976; Hawksworth and Scharpf 1986). 72 Surveys of the distribution of the EuropeanDraft mistletoe in Sonoma County were completed in 73 1971, 1986, and 1991 (Hawksworth et al. 1991). They indicated a widening host range and 74 increased annual rate of spread (.35 km/yr). However, the native upland forests of the region are 75 dominated by non-host species of oak (Quercus spp.) and conifers, interspaced with open non- 76 forested fields, groves of eucalyptus (Eucalyptus spp.), and expanding vineyards. Sharpf and 77 McCartney (1975) and Hawksworth et al. (1991) suggested that the rate of spread was slow and 78 would decline in the future because the non-hosts and landscape structure should limit the 79 spread. 80 The 1991 survey was the most recent assessment of spread for the European mistletoe in 81 Sonoma County. Because of the potential impacts this mistletoe could have on the urban and 82 natural forests of the region, another survey was conducted in 2019 to determine if the mistletoe 83 has spread significantly beyond the area where it was found in 1991. We hypothesized that by 84 2019, European mistletoe would have spread to new urban and semi-urban landscapes and due to 85 bird dispersal, might have jumped long distances to new areas of the region. This survey 4 https://mc06.manuscriptcentral.com/botany-pubs Page 5 of 26 Botany European mistletoe in California, USA 86 provides an estimate of the current distribution of European mistletoe nearly120 years after 87 introduction to California. 88 89 Methods 90 There are three mistletoes found on hardwoods in Sonoma County: European mistletoe, 91 big-leaf mistletoe (Phoradendron macrophyllum (Engelmann) Cockerell), and western oak 92 mistletoe (P. villosum (Nuttall) Nuttall) (Mathiasen and Kenaley 2016). It is possible to 93 distinguish between them because of their distinctive form, leaves and fruits. European mistletoe 94 forms distinctly spherical shrubs, the leaves are glabrous and obovate and up to 8 cm long with a 95 short petiole. The flower parts are in foursDraft and the inflorescence is a cyme with few flowers 96 formed on short peduncles. The berry is large (6-10 mm diameter) and white (Mathiasen and 97 Kenaley 2016). Big-leaf mistletoe forms large pendulous plants, has smooth leaves that are 98 obovate, elliptic-orbicular and up to 5 cm long and 3 cm wide. Western oak mistletoe forms 99 roundish shrubs, less distinctly spherical than European mistletoe, has stellate hairs on its leaves 100 and stems and its leaves are obovate-elliptic, up to 4.5 cm long and 2.2 cm wide. The flower 101 parts number in threes for big-leaf and western oak mistletoe. The berries of big-leaf mistletoe 102 are distinctly white and 4-5 mm in diameter, and the berries of western oak mistletoe are white to 103 pinkish and about 3-4 mm in diameter (Mathiasen and Kenaley 2016). Specimens of all three 104 species were deposited at the Oregon State University Herbarium (OSC), in Corvallis. 105 We surveyed for European mistletoe on February 20-22 and March 11-12, 2019 in and 106 around Sebastopol, California. Although a limited portion of the survey was conducted on foot, 107 the majority was by car. The survey began at Luther Burbank’s Gold Ridge Farm in Sebastopol, 5 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 6 of 26 European mistletoe in California, USA 108 the original point of introduction for V. album, and proceeded by driving as many miles of road 109 as possible throughout the area surrounding the perimeter of the Hawksworth et al. (1991) 110 survey. When mistletoe plants were spotted, we examined them as closely as possible; where 111 they were located on private property in urban situations, we used binoculars. When we 112 identified European mistletoe on a tree at the outer edge of the survey area, we recorded the 113 species of host tree, geographic coordinates (approximate for trees at a distance), diameter class 114 (<10 cm, 10-50 cm, or >50 cm), height class (<10 m, 10-20 m, or >20 m), relative abundance of 115 mistletoe plants (<5 plants, 5-20 plants, or >20 plants), and crown condition (poor, moderately 116 healthy, or healthy).