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
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.
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.
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). 117 Initial surveys for European mistletoeDraft in this area (McCartney et al. 1973; Hawksworth 118 and Scharpf 1986) attempted to inventory existing infected trees. By 2019, the number of trees
119 was too large and the accessibility to most of them was difficult due to the prevalence of private
120 land. Therefore, we focused our survey on locating an outer perimeter of representative infected
121 trees to find the trees located farthest away from the point of introduction. We surveyed rural
122 roadsides as well as outlying communities containing large numbers of planted hosts. The survey
123 encompassed the outlying communities of Cloverdale, Healdsburg, Sonoma, Petaluma,
124 Guerneville, and Bodega, and it ranged as far afield as the Geysers Road/Highway 101
125 intersection approximately 48 km north of the point of introduction.
126
127 Results and Discussion
128 European mistletoe incidence and distribution.
6 https://mc06.manuscriptcentral.com/botany-pubs Page 7 of 26 Botany
European mistletoe in California, USA
129 The survey noted European mistletoe infestations in many species of planted street trees
130 near the point of introduction as well as beyond the 1991 perimeter. The estimated area
131 encompassed by mistletoe-infected hosts increased from 184 km2 (71 miles2) in 1991 to 606 km2
132 (234 miles2) in 2019 (Table 1) (Fig. 3). We observed infected trees up to 24.6 km (15.3 miles)
133 from the point of introduction, double the farthest distance reported in 1991. The farthest
134 directional spread was to the southeast, along the Highway 101 corridor in Petaluma and the least
135 spread was to the west beyond Occidental. Annual rate of spread decreased somewhat between
136 1991 and 2019, as predicted by Hawksworth et al. (1991); however, it still exceeds the rate
137 reported by Hawksworth and Scharpf (1986) for the period between 1971 and 1986 (Table 1). 138 Over the past 120 years, the EuropeanDraft mistletoe has not made significant jumps to new 139 towns and valleys (Fig. 3). Sharpf and McCartney (1975) reported that the European mistletoe
140 had a slow rate of spread, while Hawksworth and Scharpf (1986) noted that the mistletoe had
141 spread rapidly on new hosts and in riparian areas to the west. Hawksworth et al. (1991) however,
142 suggested that the rates of spread of European mistletoe would decline in Sonoma County
143 because the area of susceptible hosts had largely been colonized, and non-hosts and landscape
144 structure would limit the spread. This does appear to be the case, in that the rate of spread has
145 slowed since 1991 because the mistletoe now occupies the Sebastopol/Santa Rosa basin (Fig. 3)
146 where urban/semi-urban areas have large numbers of mistletoe hosts (Table 2).
147 Near or outside the infestation perimeter, we observed thirty infected host trees and
148 collected diameter class, height class, mistletoe plant abundance, and host crown condition.
149 These trees are likely not representative of the general population of infested trees because we
150 only focused on documenting trees at the outer edge of the survey. However, most of these
151 outlying trees had only a few plants (<5), were of intermediate size (10-50 cm diameter at breast
7 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 8 of 26
European mistletoe in California, USA
152 height and 10-20 m in height), and appeared healthy (only 1 observed with poor crown health).
153 The marginal areas represent the early stages of colonization by the mistletoe, with
154 intensification likely with time.
155 European mistletoe hosts
156 European mistletoe was observed in many hardwood hosts, especially those not native to
157 California and planted in urban or semi-urban situations (Table 2) (Fig. 4). Our observations
158 increase the total number of tree species known as hosts in California to 25, with 4 genera
159 (species not determined) (Table 2). Hosts that have not been noted in previous surveys include
160 callery or Bradford pear (Pyrus calleriana Decne.), Ohio buckeye (Aesculus glabra Wild.), and 161 shagbark hickory (Carya ovata (Mill.) K.Draft Koch). Some severely infected hosts were declining 162 based on observations of dead mistletoe plants in the crown: when a branch dies, the mistletoe
163 attached to that branch dies as well (Mathiasen et al. 2008). Among these, black locust (Robinia
164 pseudoacacia L.) was one of the most frequently noted declining hosts, perhaps because these
165 are some of the original planted hardwoods in the area.
166 European mistletoe was observed infecting several riparian trees in Sonoma County,
167 including Oregon ash, Pacific willow (Salix lasiandra Benth.), cottonwood (Populus sp.), red
168 alder (Alnus rubra Bong.), and bigleaf maple (Acer macrophyllum Pursh) (Table 2). It appears
169 that for native plant communities, riparian areas of Sonoma County are the habitat most
170 susceptible to European mistletoe infestations because upland communities do not have many
171 host trees. We therefore, recommend that future surveys focus on surveying riparian areas.
172 Although we did not see any trees in decline within riparian areas, we observed some trees with
173 many mistletoe plants.
8 https://mc06.manuscriptcentral.com/botany-pubs Page 9 of 26 Botany
European mistletoe in California, USA
174 We also noted an infection in northern red oak (Quercus rubra L.), the only infection of
175 an oak tree by European mistletoe known in California. European mistletoe rarely occurs on oaks
176 (Quercus spp.) in Europe. The rare occurrence on oak in England was once used as an indication
177 that the tree and place were special and sacred. Some thought the mistletoe plant that grew in
178 oaks would heal the sick, while legends abound about the use of mistletoe (Lev et al. 2011).
179 Recently, Box (2019) surveyed the United Kingdom for the occurrence of European mistletoe on
180 oak. Box found 11 known locations, with the trees highly regarded and their status tracked in
181 historical records. In France, a much larger number of oaks are known to be infected by
182 European mistletoe, including non-native oaks from North America. Our detection of European
183 mistletoe on northern red oak in eastern Sonoma County appears to be the only location in North
184 America where European mistletoe has Draftbeen observed infecting an oak.
185 The upland vegetation of Sonoma County includes non-host conifers, dominated by
186 redwood (Sequoia sempervirens (Lamb. Ex D. Don) Endl.) and Douglas-fir (Pseudotsuga
187 menziesii (Mirb.) Franco), as well as numerous native oaks, including coast live oak (Quercus
188 agrifolia Née) valley oak (Q. lobata Née), Oregon white oak (Q. garryana Douglas ex Hook.),
189 and California black oak (Q. kelloggii Newberry). The landscape is a mix of natural upland
190 forests, riparian forests, farms, towns/yards, cities, open pasture and agricultural plantings (Fig.
191 5). Vineyards are increasingly common and replacing apple and fruit tree orchards. Although
192 some aspects of the landscape limit spread, other settings facilitate spread and intensification
193 such as urban streets lined with maples. The habitat for European mistletoe likely includes farm
194 – city non-native vegetation, semi-rural yards, and city streets where many susceptible hosts
195 occur, such as black locust, planted maples (Acer rubrum L. and A. saccharinum L.), poplars
196 (Populus spp.), apples (Malus spp.), and pears (Pyrus spp.).
9 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 10 of 26
European mistletoe in California, USA
197 Other leafy mistletoes in Sonoma County urban settings
198 We also observed two additional native leafy mistletoes, western oak mistletoe and big-
199 leaf mistletoe widely distributed in the survey area especially in some urban settings. We
200 observed western oak mistletoe on oaks (Quercus spp.), with particularly severe infestations on
201 species in the non-native red oak group, such as pin oak (Q. palustris Münchh.). We observed
202 big-leaf mistletoe on other hardwood species, especially species typically associated with
203 riparian zones such as Oregon ash and Northern California walnut (Juglans hindsii (Jeps.) Jeps.
204 Ex R. E. Sm.) and also some non-native hardwoods such as black locust. Big-leaf mistletoe
205 appears to be widely distributed in communities along the Russian River and Sonoma Creek 206 watersheds; all mistletoe infestations observedDraft in the communities of Ukiah, Hopland, 207 Cloverdale, and Sonoma were populations of big-leaf mistletoe.
208
209 Dispersal Agents
210 During our survey we observed avian foraging on European mistletoe berries once. This
211 was a large (~60 individuals), active, and tight flock of cedar waxwings (Bombycilla cedrorum
212 Vieillot, 1808). The flock was foraging on berries, moving between perches and feeding. When
213 alarmed, flew off in one large tightly aggregated flock. Hawksworth and Scharpf (1986) state
214 cedar waxwings and American robins (Turdus migratorius Linnaeus, 1766) are known to eat the
215 berries of European mistletoe in California, and that the cedar waxwings are likely the most
216 important dispersal agent: “…great flocks have been observed avidly feeding on ripe European
217 mistletoe berries from January through March”. Cedar waxwings are almost 100% frugivorous
218 in winter (Witmer 1996), and are probably an important European mistletoe dispersal agent.
10 https://mc06.manuscriptcentral.com/botany-pubs Page 11 of 26 Botany
European mistletoe in California, USA
219 McPherson (1987) studied cedar waxwing winter diet in Oklahoma, where they fed almost
220 exclusively on Phoradendron leucarpum (Rafinesque) Reveal & M. C. Johnston until the fruit
221 was depleted. In Sonoma County, cedar waxwings may serve to assist in intensification and
222 local spread of European mistletoe due to their intense and local feeding.
223
224 Management recommendations
225 European mistletoe is established in Sonoma County. This raises the question: is this non-
226 native parasitic plant a threat to urban and forest trees in California? We did not undertake
227 studies of impacts on tree health and only observed declining trees associated with European 228 mistletoe in a few locations. Sharpf andDraft McCartney (1975) noted that the European mistletoe 229 was not considered a serious economic pest because it had limited impacts to orchards and a
230 slow rate of spread. However, as noted by Hawksworth and Scharpf (1991), European mistletoe
231 is known as a serious tree disease agent in some parts of Europe, with a large host range of over
232 450 species of trees (Barney et al. 1998). The potential for mistletoe intensification and declines
233 of host trees is certainly there for some tree species in Sonoma County. Since mistletoe plants
234 require a live host and do not persist on dead material, management can involve pruning infected
235 branches or killing the host tree to eradicate it locally (Shaw and Mathiasen 2013). Currently, the
236 European mistletoe is being managed in urban areas (Fig. 6) and this will likely continue within
237 the infested area. We recommend eradication of the mistletoe when new locations are found in
238 cities beyond the current infestation area. For example, we found two lone plants in Petaluma
239 and suggest it would be good to prune these plants. Finally, we feel natural area managers
240 should consider eradication efforts in riparian areas if new infestations are found. Controlling
241 the vectors is an assault on native birds and unlikely to succeed.
11 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 12 of 26
European mistletoe in California, USA
242 We support the recommendation of Hawksworth and Sharpf (1991) that this mistletoe
243 infestation be monitored every 5 to 10 years to keep track of the rate of spread and determine if it
244 jumps longer distances to nearby towns and cities. The most critical threat to native plant
245 communities in Sonoma County from European mistletoe is the potential for spread and
246 intensification in riparian forests. Most trees within these forests are hosts, and within the current
247 infestation we observed some wetland forest and riparian area trees with severe infection, such as
248 near Graton and Forestville. European mistletoe spread west toward Bodega appears to be mostly
249 in native riparian areas especially on red alder (Hawksworth and Scharpf 1986). As the climate
250 dries and the temperature increases in California, the European mistletoe may become more
251 limited to urban and suburban areas due to landscape watering, while longer growing seasons
252 and hotter drought may put greater stressDraft on riparian trees with existing infections (Bell et al.
253 2019).
254
255 Acknowledgements
256 We thank Oregon State University and California Department of Forestry and Fire
257 Protection for supporting this study.
258
259 Literature cited
260 Barney, C.W., Hawksworth, F.G., and Geils, B.W. 1998. Hosts of Viscum album. Eur. J. For.
261 Pathol. 28: 187-208.
12 https://mc06.manuscriptcentral.com/botany-pubs Page 13 of 26 Botany
European mistletoe in California, USA
262 Bell, D.M., Pabst, R.J., and Shaw, D.C. 2019. Tree growth declines and mortality were
263 associated with a parasitic plant during warm and dry climatic conditions in a temperate
264 coniferous forest ecosystem. Global Change Biol. 2019: 00: 1-11.
265 DOI:10.1111/gcb.14834.
266 Box, J. 2019. Mistletoe Viscum album L. (Loranthaceae) on oaks in Britain. Watsonia, 23: 237-
267 256.
268 Butin, H. 1995. Tree Diseases and Disorders. Oxford University Press, Oxford, UK.
269 Dorworth, C.E. 1989. European Mistletoe (Viscum album subsp. album) in Canada. Plant Dis.
270 73:444. DOI: 10.1094/PD-73-0444E.
271 Esri. 2012. "World Topographic" [basemap].Draft Scale 1:185,627. "World Topographic Map".
272 http://www.arcgis.com/home/item.html?id=30e5fe3149c34df1ba922e6f5bbf808f.
273 Accessed February 14, 2020.
274 Freuding, M., Keinki, C., Micke, O, Buentzel, J., and Huebner, J. 2019. Mistletoe in oncological
275 treatment: a systematic review Part 1: survival and safety. J. Cancer Res. Clin. Oncol.
276 145: 695-707. DOI: 10.1007/s00432-018-02837-4
277 Hawksworth, F.G. 1983. Mistletoes as forest parasites. In The Biology of Mistletoes. Edited by
278 M. Calder and P. Bernhardt. Academic Press, Sydney, Australia pp. 317-333.
279 Hawksworth, F.G., and Scharpf, R.F. 1986. Spread of European mistletoe (Viscum album) in
280 California, U.S.A. Eur. J. For. Pathol. 16: 1-5.
281 Hawksworth, F.G., Scharpf, R.F., and Marosy, M. 1991. European mistletoe continues to spread
282 in Sonoma County. California Agriculture, November-December 1991: 39-40.
13 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 14 of 26
European mistletoe in California, USA
283 Kope, H. H. in press. European mistletoe (Viscum album subsp. album) in Victoria, British
284 Columbia, Canada: an eradication follow-up. Canadian Plant Disease Survey.
285 Lev, E., Ephraim, M., and Ben-Arye, E. 2011. European and Oriental mistletoe: from
286 mythology to contemporary integrative cancer care. European Journal of Integrative
287 Medicine, 3: el33-el37.
288 Mathiasen, R.L., and Kenaley, S.C. 2016. The classification of California Viscaceae: an
289 alternative perspective. Madroño, 63:8-33.
290 Mathiasen, R.L., Nickrent, D.L., Shaw, D.C., and Watson, D.M. 2008. Mistletoes: pathology,
291 systematics, ecology, and management. Plant Dis. 92: 988-1006.
292 McCartney, W.O. 1968. European mistletoe,Draft Viscum album, an unusual phanerogamic parasite
293 in California. Plant Disease Reporter, 52: 198-201.
294 McCartney, W.O., Scharpf, R.F., and Hawksworth, F.G. 1973. Additional hosts of Viscum
295 album, European mistletoe, in California. Plant Disease Reporter, 57: 904.
296 McPherson, J.M. 1987. A field study of winter fruit preferences of cedar waxwings. The
297 Condor, 89: 293-306.
298 Pandora, K. 2001. Knowledge Held in Common: Tales of Luther Burbank and Science in the
299 American Vernacular, Isis 92: 484-516. https://doi.org/10.1086/385279
300 Scharpf, R.F., and Hawksworth, F.G. 1976. Luther Burbank introduced European mistletoe into
301 California. Plant Disease Reporter, 60: 740-742.
302 Scharpf, R.F., and McCartney, W. 1975. Viscum album in California – its introduction,
303 establishment and spread. Plant Disease Reporter, 59: 257-262.
14 https://mc06.manuscriptcentral.com/botany-pubs Page 15 of 26 Botany
European mistletoe in California, USA
304 Shaw, D.C., and Mathiasen, R.L. 2013. Management of Higher Parasitic Plants – Mistletoes. In
305 Infectious Forest Diseases. Edited by G. Nicolotti and P. Gonthier. CABI Press,
306 Oxfordshire, U.K. pp. 97-114.
307 Zuber, D. 2004. Biological flora of Central Europe: Viscum album L. Flora, 199: 181-203.
308 Witmer, M.C. 1996. Annual diet of cedar waxwings based on U.S. Biological Survey Records
309 (1885-1950) compared to diet of American robins: contrasts in dietary patterns and
310 natural history. The Auk, 113: 414-430.
311
312 Draft
15 https://mc06.manuscriptcentral.com/botany-pubs Botany Page 16 of 26
European mistletoe in California, USA
313 Figure Captions
314 Figure 1. The European mistletoe, female plant with berries in January, Sonoma County,
315 California, USA.
316 Figure 2. The European mistletoe in apple (Malus sp.) in Sonoma County California, January,
317 2019.
318 Figure 3. Map of outer edge of known infestation area for European mistletoe in 1991 (yellow
319 circles) and 2019 (red circles) in Sonoma County, California, USA (Hawksworth et al. 1991;
320 ESRI 2012). Figure constructed using ArcGIS Desktop 10.6.1.
321 Figure 4. The European mistletoe in poplar, Sebastopol, Sonoma County, California, USA. Draft 322 Figure 5. Landscape setting south of Santa Rosa, looking east across the Penngrove subdivision.
323 Note native vegetation in mountains on the horizon, the patchiness of the forested landscape and
324 the trees in the foreground, which are Eucalpytus, are not susceptible. The core habitat for
325 European mistletoe is the urban setting in the central part of the photo.
326 Figure 6. Management of European mistletoe by removing aerial shoots and wrapping with
327 plastic in Sebastopol, California.
328
16 https://mc06.manuscriptcentral.com/botany-pubs Page 17 of 26 Botany
Tables
Table 1. Spread of European mistletoe since 1900, from its point of introduction in Sebastopol,
Sonoma County, California, USA. 1971, 1986, 1991 survey data from Hawksworth et al.
(1991).
Year Distance: range Distance: Annual rate of Approximate
in km (miles) average in km spread km/yr gross area in
(miles) (miles/yr) km2 (square
miles)
1971 1.2 – 4.5 2.4 0.03 26 (0.8 – 2.8) Draft(1.5) (0.02) (10) 1986 3.5 – 12.1 6.3 0.26 163
(2.2-7.5) (3.9) (0.16) (63)
1991 4.3 – 12.1 8.0 0.35 184
(2.7-7.5) (5.0) (0.22) (71)
2019 9.5-24.6 15.8 0.27 606
(5.9-15.3) (9.8) (0.17) (234)
https://mc06.manuscriptcentral.com/botany-pubs Botany Page 18 of 26
Table 2. List of host tree species known for European mistletoe in Sonoma County California.
*species observed in 2019 new to the 1991 list (from Hawkworth et al. 1991). Authorities for taxonomic names checked on Integrated Taxonomic Information System (ITIS, US Geological
Survey and Smithsonian Institution) website: https://www.itis.gov/ (checked December 24,
2019)
Native Species (7)
Scientific name Common name Family
Acer macrophyllym Pursh bigleaf maple Aceraceae
Alnus rubra Bong. red alder Betulaceae Aesculus californica (Spach) CaliforniaDraft buckeye Hippocastanaceae Nutt
*Fraxinus latifolia Benth Oregon ash Oleaceae
Populus fremontii S. Watson Fremont’s cottonwood Salicaceae
*Populus trichocarpa Torr.& black cottonwood Salicaceae
A. Gray ex Hook.
Salix lasiandra Benth. Pacific willow Salicaceae
Introduced (non-native to
Sonoma County) trees (18 species and 4 genera without species identification)
Scientific name Common name Family
*Acer rubrum L. red maple Aceraceae
https://mc06.manuscriptcentral.com/botany-pubs Page 19 of 26 Botany
Acer saccharinum L. silver maple Aceraceae
Acer saccharum Marsh. sugar maple Aceraceae
*Aesculus glabra Wild. Ohio buckeye Hippocastanaceae
Betula pendula Roth European white birch Betulaaceae
Diospyros kaki Thunb. Japanese persimmon Ebenaceae
*Carya ovata (Mill.) K. Koch shagbark hickory Juglandaceae
Fraxinus velutina Torr. velvet ash Olacaceae
Crataegus sp. hawthorn Rosaceae
Malus sp. Cultivated apple Rosaceae
Malus floribunda Siebold ex Japanese flowering crabapple Rosaceae
Van Houtte Draft
Populus alba L. white poplar, also reported on Salicaceae
Bolleana poplar
Populus nigra L. reported on Lombardy poplar Salicaceae
Prunus salicina Lindl. Japanese or Santa Rosa plum Rosaceae
Pyracantha sp. Pyracantha Rosaceae
*Pyrus calleryana Decne. Callery pear Rosaceae
*Quercus rubra L. northern red oak Fagaceae
Robinia pseudoacacia L. black locust Fabaceae
Sorbus aucuparia L. European mountain-ash Rosaceae
Salix babylonica L. weeping willow Salicaceae
Salix discolor Muhl. pussy willow Salicaceae
Ulmus sp. Elm Ulmaceae
https://mc06.manuscriptcentral.com/botany-pubs Botany Page 20 of 26
Draft
https://mc06.manuscriptcentral.com/botany-pubs Page 21 of 26 Botany
Draft
https://mc06.manuscriptcentral.com/botany-pubs Figure 1. Botany Page 22 of 26
Draft
Figure 2. https://mc06.manuscriptcentral.com/botany-pubs Page 23 of 26 Botany
Draft
Figure 3.https://mc06.manuscriptcentral.com/botany-pubs Botany Page 24 of 26
Draft
https://mc06.manuscriptcentral.com/botany-pubs Figure 4. Page 25 of 26 Botany
Draft
Figure 5. https://mc06.manuscriptcentral.com/botany-pubs Botany Page 26 of 26
Draft
Figure 6. https://mc06.manuscriptcentral.com/botany-pubs